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Temperature-dependent development of Ophyra aenescens (Wiedemann, 1830) and Ophyra capensis (Wiedemann, 1818) (Diptera, Muscidae)
Forensic Science International 139 (2004) 75–79
Temperature-dependent development of Ophyra aenescens (Wiedemann, 1830) and Ophyra capensis (Wiedemann, 1818) (Diptera, Muscidae) Fabrice Lefebvre, Thierry Pasquerault* Institut de Recherche Criminelle de la Gendarmerie Nationale, 1 Bd The´ophile Sueur, 93111 Rosny-sous-Bois Cedex, France Received 28 May 2003; accepted 23 October 2003
Abstract The influence of rearing temperature on the development rates of two ‘‘dump flies’’ Ophyra aenescens (Wiedemann, 1830) and Ophyra capensis (Wiedemann, 1818) is analysed. The development times of these species are determined. Flies were reared at three constant temperatures (17 1, 24 1 and 30 1 8C) with a photoperiod of 12:12 and at a relativity moisture of 75– 95%. The minimum duration for each development stages, from eggs to pupae and from eggs to adult emergence of O. aenescens and O. capensis are reported. The development rate increases in both species as the rearing temperature rises. A temperaturedependent development model is calculated for each species. The larval and total development of these two species can be estimated if the environmental temperature is between 17 and 30 8C. Compared to O. aenescens, O. capensis has a higher threshold of development and a longer larval development time. # 2003 Elsevier Ireland Ltd. All rights reserved. Keywords: Ophyra aenescens; Ophyra capensis; Forensic entomology; Temperature-dependent; Development rate
1. Introduction
2. Materials and methods
Forensic entomology can help to estimate the time elapsed since death, the so-called ‘‘Post-Mortem Interval’’ (PMI) [1]. One such method consists of determining the age of dipteran larvae collected from the corpse [2–4]. Therefore, it is essential for forensic entomologists to know precisely the rate of development of the different necrophagous species (Diptera). Insect development is affected by many things and in particular the environmental conditions. Temperature is the most important factor affecting development rate [5]. The aim of this paper is to establish a new model of development depending on temperature of two sapro-necrophagous species of the Muscidae (Diptera, Brachycera).
The species studied belong to the ‘‘dump flies’’ or the ‘‘black garbage flies’’ (Diptera, Muscidae): Ophyra aenescens (Wiedemann, 1830) and Ophyra capensis (Wiedemann, 1818). The genera Ophyra and Hydrotaea were described in 1830 by Robineau-Desvoidy. Several authors consider that they are synonymous [6], but the majority think that both Ophyra and Hydrotaea are valid [7,8]. These species are often associated with poultry and swine houses where the larvae grow in garbage and manure, which both have wide moisture range [9]. O. capensis is frequently associated with the necrophagous fauna on animal and human cadavers. ‘‘Dump fly’’ larvae can be facultative predators of larvae of other fly species, but others have a normal development without predation behaviour [7,9,10]. Larval supplies of O. aenescens were bought in a fishing tackle shop. The strains come from the south of France (region of Languedoc-Roussillon). O. capensis was captured near Paris using a flower-pot trap.
* Corresponding author. Tel.: þ33-1-49-35-5862; fax: þ33-1-49-35-5027. E-mail address: [email protected] (T. Pasquerault).
0379-0738/$ – see front matter # 2003 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.forsciint.2003.10.014
76
F. Lefebvre, T. Pasquerault / Forensic Science International 139 (2004) 75–79
plete development were calculated for both species. The total accumulated degree-days needed for larval and complete development at one rearing temperature (ADDi) was calculated from the equation: ADDi ¼ n(TiTs); n is the number of development days; Ti the rearing temperature; Ts is the lower development threshold. The thermal constant was calculated for each of the three constant temperatures (for larval and complete development) to obtain the average ADDT ðmean s2 Þ.
Adults were reared at our laboratory in at room temperature (20 2 8C) and under natural photoperiod for 2 years. For each species, 200 adults were kept in a plastic cage (300 mm 500 mm 500 mm) and provided with sugar and water [11,12]. Adults were allowed to oviposit on the surface of fresh beef muscle of uniform quality [12,13]. The meat was observed several times a day. As soon as eggs had been laid, the meat was transferred in a plastic box (260 mm 130 mm 77 mm) containing a layer of sand (30 mm thick) for larval development. These boxes were put in a FIRLABO SPE 140 H incubator. Larval development took place in a relative humidity of between 75 and 95% and a photoperiod of 12:12 h. Three constant temperature regimes were used: 17 1, 24 1 and 30 1 8C. 24 8C is the temperature chosen by the French Forensic Entomology Department to rear specimens collected at the crime scene or the autopsy. The two other temperatures were chosen because they represent the highest and lowest limits of our incubator to allow an accuracy of 1 8C. The eggs were never directly handled. During larval growth and the pupal stage, the specimens were regularly observed (two to three times per day). The first appearance of different development stages (first, second and third larval instars and puparial stage) was noted for O. aenescens. The percentages of time taken by each stage were calculated and the minimum durations of larval and puparial development were determined. The minimum durations of larval and pupal development were also determined for O. capensis. The numbers of breeding (i), the mean (m), the standard deviation (s2) and the modes (M) of the minimum duration of the larval and the total development were determined. Campbell et al. [14], and Grassberger and Reiter [15,16] reported that the development of insects can be described using temperature summation, the accumulation degreedays (ADD) model. It is only valid for the linear portion of the sigmoid development curve. The minimum threshold of development (Ts) for each species was calculated from a linear regression (Microsoft1 Excel 98) of the development rates (t ¼ 1/development time) following the constant temperature: t ¼ f(T8C). Values Ts of the larval and the com-
3. Results 3.1. Ophyra aenescens (Wiedemann, 1830) This species is easily reared in laboratory conditions, a maximum of viable eggs is usually laid on the substrate (beef meat). During the larval growth the duration of the development period decreased as the rearing temperature increased. For each temperature, the minimum duration of the larval development, was measured with six replicates. The total development was measured with 7 replicates at 17 8C, 23 at 24 8C and 11 at 30 8C. For each replicate and rearing temperature regime, the first appearance of the different larval stages, the first puparium and the first adult emergence were noted. The minimum duration at each development stage and the minimum duration of total development at each temperature regime are given in Table 1. The percentage of time taken by each stage is also calculated. The minimum duration of the egg incubation is about 5– 6% of the total development period. The first and second larval stages are sub equal and each of them represents about 10–12% of the total development time. The minimum duration of the puparial stage is as long as the total larval development one. Overall, the duration of the different stages of development decreases as the rearing temperature rises. The average minimum larval and total time of development of this species are presented in Table 2. The minimum duration of larval development is 1.90 times longer at 17 8C
Table 1 Minimum duration of the development stages of O. aenescens (in hours) Stage
17 1 8C
24 1 8C
30 1 8C
First appearance
%
First appearance
%
First appearance
%a
Egg First instars Second instars Third instarsb Pupalc
48 98 88 198 393
6 12 11 24 47
20 46 40 124 168
5 12 10 31 42
14 24 24 80 130
5 9 9 29 48
Total
825
–
398
–
272
–
a
Percentage of total development time. b Post-feeding stage included. c Puparation to emergence.
a
a
F. Lefebvre, T. Pasquerault / Forensic Science International 139 (2004) 75–79
77
Table 2 Average minimum duration of larval and total development of O. aenescens (in days) 17 1 8C
Larval development Total development
24 1 8C 2
30 1 8C 2
M
n
m
s2
M
9 17
11 11
6.6 12.4
0.69 0.74
6 12
n
m
s
M
n
m
s
6 7
18.2 37.1
2.48 4.71
19 nsa
22 23
9.5 17.6
1.46 1.87
n: number of breeding; m: average minimum duration; s2: standard deviation; M: mode. a Missing data.
Fig. 1. Linear regression of the larval and total development of O. aenescens.
than at 24 8C, 2.77 times longer at 17 8C than at 30 8C and 1.45 times longer at 24 8C than at 30 8C. The minimum duration of a complete cycle is 2.11 times longer at 17 8C than at 24 8C, 2.99 times longer at 17 8C than at 30 8C and 1.42 times longer at 24 8C than at 30 8C. The relationship between the development rate of O. aenescens and rearing temperature is shown in Fig. 1. Larval development rates are 0.06, 0.11 and 0.15, respectively at 17, 24 and 30 8C. The equation of the regression line is y ¼ 0:0069x 0:0573 ðR2 ¼ 0:9996Þ where y is the development rate and x is the rearing temperature. The minimum threshold Ts for the larval development is 8.3 8C and the thermal constant ADDL is 149:90 7:98 degree-days above Ts. Total development rates are 0.03, 0.06 and 0.08, respectively at 17, 24 and 30 8C. The linear regression of development rate from egg to adult is y ¼ 0:0039x 0:0346 ðR2 ¼ 0:995Þ. The minimum threshold Ts for the total development is 8.9 8C and the thermal constant ADDT is 276:10 21:50 degree-days above Ts. 3.2. Ophyra capensis (Wiedemann, 1818) Compared with O. aenescens, the duration of development is shortened when the constant rearing temperature is higher but the mortality is more important that of O. aenescens (unpublished data). That is the reason why, during the experiments, disturbance was kept to a minimum. The duration of each larval stage was not studied in this species. To determine the minimum duration of the larval development, 11 replicates were run at 17 8C, 19 at 24 8C and 18 at
30 8C. For the minimum duration of the total development, 8 replicates were run at 17 8C, 19 at 24 8C and 16 at 30 8C. The minimum larval and total time of development of this species are given in Table 3. The minimum duration of larval development is 2.86 times longer at 17 8C than at 24 8C, 5.42 times longer at 17 8C than at 30 8C and 1.89 times longer at 24 8C than at 30 8C. The minimum duration of a complete cycle is 2.95 times longer at 17 8C than at 24 8C, 4.96 times longer at 17 8C than at 30 8C and 1.68 times longer at 24 8C than at 30 8C. The development rates of O. capensis, at different experimental temperatures, are shown in Fig. 2. The larval development rates are 0.03, 0.08 and 0.14, respectively at 17, 24 and 30 8C. The equation of the regression line is y ¼ 0:0084x 0:1161 ðR2 ¼ 0:9907Þ where y is the development rate and x is the rearing temperature. The minimum threshold Ts for the larval development is 13.8 8C and the thermal constant ADDL is 123:32 11:06 degree-days above Ts. The rates of total regression are 0.02, 0.05 and 0.08, respectively at 17 1, 24 1 and 30 1 8C. The linear regression of development rate from egg to adult is y ¼ 0:0046x 0:059 ðR2 ¼ 0:998Þ. The minimum threshold Ts of total development is 12.8 8C and the thermal constant ADDT is 237:05 22:73 degree-days above Ts.
4. Discussion Species of ‘‘dump flies’’, such as O. aenescens, are often used as a biological control agent of the house fly Musca
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F. Lefebvre, T. Pasquerault / Forensic Science International 139 (2004) 75–79
Table 3 Average minimum duration of larval and total development of O. capensis (in days) 17 1 8C
Larval development Total development
24 1 8C 2
30 1 8C 2
M
n
m
s2
M
12 21
18 16
7.0 12.5
0.77 0.82
7 13
n
m
s
M
n
m
s
11 8
37.9 62.0
4.53 5.53
34 nsa
19 19
13.3 21.1
1.28 2.01
n: number of breeding; m: average minimum duration; s2: standard deviation; M: mode. a Missing data.
Fig. 2. Linear regression of the larval and total development of O. capensis.
domestica Linneaus, 1758 in poultry houses. Their biology and behaviour are well documented. Johnson and Venard have shown that O. aenescens has a generation time of 14 days at 26:5 1 8C [17]. In contrast, Schuman has reported that the same cycle ended in 8 days at 23 8C [18]. Our study shows that complete development of O. aenescens takes 17:6 1:87 days at 24 8C. Using the thermal development model, the durations of the total development of this species were estimated in 19:6 1:5 days at 23 8C and in 15:7 1:2 days at 26.5 8C. These results are similar to those obtained by Johnson and Venard but they differ greatly of those reported by Schuman. In both cases however, some differences in the development times remain. The development of insects depends on numerous factors including the experimental conditions of rearing. The variation of the photoperiod or relative humidity or larval development substrate could explain the different duration of development times observed. The geographic origin of the populations could be considered as another factor that may also partly explain these differences. Grassberger and Reiter [15,16], and Greenberg [19] assumed that the fly necrophagous species presented geographic variation and adaptation. Their development times may differ under the same environmental conditions according to the population studied. Likewise, under the same rearing conditions, the duration of the larval development of O. capensis could be longer that of O. aenescens. For O. aenescens, the percentage of duration of the larval development is 50%. It is 60% for O. capensis. The development threshold Ts of O. capensis is higher than the Ts of O. aenescens. These results suggest that
O. capensis requires milder temperature conditions to develop properly as O. aenescens. They also show that the optimal development temperature of O. capensis is higher than O. aenescens one [6]. Little data is known about O. capensis and in particular its biology is poorly documented. However, they are important for forensic entomology because these species may be associated with human cadavers. O. capensis is frequently identified by our unit; 10% of the cases studied since 1992 [20] contain that species.
5. Conclusion The temperature-dependent development models of O. aenescens and O. capensis are determined for rearing temperature included between 17 and 30 8C corresponding to the linear sections of the sigmoid development curve models for these species. These experiments were carried out in constant temperatures. In forensic entomology, this situation is similar to an indoor crime scene. Outdoors, the quality of the temperature records will be important in allowing these data to be of value in the Post-Mortem Interval investigation.
Acknowledgements We thank very much Benoıˆt Vincent and Emmanuel Carcreff for their great help to carry out these experiments. We thank also Emmanuel Gaudry, Laurent Dourel, Bernard Chauvet and Jean-Bernard Myskowiak for their constant
F. Lefebvre, T. Pasquerault / Forensic Science International 139 (2004) 75–79
assistance. Special thanks to Bryan Turner for his great help. Lastly, we are very grateful to Yvan Malgorn and Frederic Brard for their precious advices.
References [1] K.G.V. Smith, A Manual of Forensic Entomology, British Museum (Natural History), London, UK, 1986, 205 pp. [2] E.P. Catts, N.H. Haskell, Entomology & Death: A Procedural Guide, Joyce’s Print Shop Inc., Clemson, SC, USA, 1990, 182 pp. [3] J.D. Wells, L.R. LaMotte, Estimating the post-mortem interval, in: J.H. Byrd, J.L. Castner (Eds.), Forensic Entomology: The Utility of Arthropods in Legal Investigations, CRC Press, Boca Raton, FL, USA, 2001, pp. 263–285. [4] B. Greenberg, J.C. Kunich, Entomology and the Law: Flies as Forensic Indicators, Cambridge University Press, Cambridge, UK, 2002, 306 pp. [5] J.-B. Myskowiak, C. Doums, Effects of refrigeration on the biometry and development of Protophormia terraenovae (Robineau-Desvoidy) (Diptera: Calliphoridae) and its consequences in estimating post-mortem interval in forensic investigations, Forensic Sci. Int. 125 (2002) 254–261. [6] A.C. Pont, Family muscidae, in: A.S. So´ os. L. Papp (Eds.), Catalog of the Palearctic Diptera, vol. 11, Hungarian Natural Museum, Budapest, 1986, pp. 57–215. [7] P. Skidmore, The Biology of the Muscidae of the World, Dr. W. Junk Publisher, Dordrecht, The Netherlands, 1985, 550 pp. [8] C.J.B. de Carvalho, Muscidae (Diptera) of the Neotropical Region: Taxonomy, Editora UFPR, Curitibia, Brasil, 2002, 287 pp. [9] J.A. Hogsette, R. Farkas, R.R. Coler, Development of Hydrotaea aenescens (Diptera: Muscidae) in manure of unweaned dairy calves and lactating cows, J. Econ. Entomol. 95 (2002) 527–530.
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[10] T. Olckers, P.E. Hulley, Facultative predation of house fly larvae by larvae of Ophyra capensis (Wiedemann) (Diptera: Muscidae), J. Entomol. Soc. S. Afr. 47 (1984) 231–237. [11] G.S. Anderson, Minimum and maximum development rates of some forensically important Calliphoridae (Diptera), J. Forensic Sci. 45 (1999) 824–832. [12] J.H. Byrd, Laboratory rearing of forensic importance, in: J.H. Byrd, J.L. Castner (Eds.), Forensic Entomology: The Utility of Arthropods in Legal Investigations, CRC Press, Boca Raton, FL, USA, 2001, pp. 121–142. [13] N.H. Haskell, Entomological collection techniques at autopsy and for specific environments, in: E.P. Catts. N.H. Haskell (Eds.), Entomology & Death: A Procedural Guide, Joyce’s Print Shop Inc., Clemson, SC, USA, 1990, pp. 98–110. [14] A. Campbell, B.D. Frazer, N. Gilbert, A.P. Gutierrez, M. Mackauer, Temperature requirements of some aphids and their parasites, J. Appl. Ecol. 11 (1974) 431–438. [15] M. Grassberger, C. Reiter, Effect of temperature on development of the forensically important holarctic blow fly Protophormia terraenovae (Robineau-Desvoidy) (Diptera: Calliphoridae), Forensic Sci. Int. 128 (2002) 177–182. [16] M. Grassberger, C. Reiter, Effect of temperature on development of Liopygia (¼ Sarcophaga) argyrostoma (Robineau-Desvoidy) (Diptera: Sarcophagidae) and its forensic implications, J. Forensic Sci. 47 (2002) 1332–1336. [17] W.T. Johnson, C.E. Venard, Observations on the biology and morphology of Ophyra aenescens (Diptera: Muscidae), Ohio J. Sci. 57 (1957) 21–26. [18] H. Schuman, Zur Bedeutung des Musca domestica, Antagonisten Ophyra aenescens (Diptera: Muscidae), II. Morphologie der Entwicklungsstadien, Angew. Parasitol. 23 (1982) 86–92. [19] B. Greenberg, Flies as forensic indicators, J. Med. Entomol. 28 (1991) 565–577. [20] J.B. Myskowiak, B. Chauvet, T. Pasquerault, C. Rocheteau, J.-M. Vian, Synthe`se de six anne´ es d’activite´ en entomologie me´ dico-le´ gale - L’inte´ reˆ t des insectes ne´ crophages en police judiciaire, Ann. Soc. Entomol. Fr. 35 (1999) 569–572.
Temperature-dependent development of Ophyra aenescens (Wiedemann, 1830) and Ophyra capensis (Wiedemann, 1818) (Diptera, Muscidae) Fabrice Lefebvre, Thierry Pasquerault* Institut de Recherche Criminelle de la Gendarmerie Nationale, 1 Bd The´ophile Sueur, 93111 Rosny-sous-Bois Cedex, France Received 28 May 2003; accepted 23 October 2003
Abstract The influence of rearing temperature on the development rates of two ‘‘dump flies’’ Ophyra aenescens (Wiedemann, 1830) and Ophyra capensis (Wiedemann, 1818) is analysed. The development times of these species are determined. Flies were reared at three constant temperatures (17 1, 24 1 and 30 1 8C) with a photoperiod of 12:12 and at a relativity moisture of 75– 95%. The minimum duration for each development stages, from eggs to pupae and from eggs to adult emergence of O. aenescens and O. capensis are reported. The development rate increases in both species as the rearing temperature rises. A temperaturedependent development model is calculated for each species. The larval and total development of these two species can be estimated if the environmental temperature is between 17 and 30 8C. Compared to O. aenescens, O. capensis has a higher threshold of development and a longer larval development time. # 2003 Elsevier Ireland Ltd. All rights reserved. Keywords: Ophyra aenescens; Ophyra capensis; Forensic entomology; Temperature-dependent; Development rate
1. Introduction
2. Materials and methods
Forensic entomology can help to estimate the time elapsed since death, the so-called ‘‘Post-Mortem Interval’’ (PMI) [1]. One such method consists of determining the age of dipteran larvae collected from the corpse [2–4]. Therefore, it is essential for forensic entomologists to know precisely the rate of development of the different necrophagous species (Diptera). Insect development is affected by many things and in particular the environmental conditions. Temperature is the most important factor affecting development rate [5]. The aim of this paper is to establish a new model of development depending on temperature of two sapro-necrophagous species of the Muscidae (Diptera, Brachycera).
The species studied belong to the ‘‘dump flies’’ or the ‘‘black garbage flies’’ (Diptera, Muscidae): Ophyra aenescens (Wiedemann, 1830) and Ophyra capensis (Wiedemann, 1818). The genera Ophyra and Hydrotaea were described in 1830 by Robineau-Desvoidy. Several authors consider that they are synonymous [6], but the majority think that both Ophyra and Hydrotaea are valid [7,8]. These species are often associated with poultry and swine houses where the larvae grow in garbage and manure, which both have wide moisture range [9]. O. capensis is frequently associated with the necrophagous fauna on animal and human cadavers. ‘‘Dump fly’’ larvae can be facultative predators of larvae of other fly species, but others have a normal development without predation behaviour [7,9,10]. Larval supplies of O. aenescens were bought in a fishing tackle shop. The strains come from the south of France (region of Languedoc-Roussillon). O. capensis was captured near Paris using a flower-pot trap.
* Corresponding author. Tel.: þ33-1-49-35-5862; fax: þ33-1-49-35-5027. E-mail address: [email protected] (T. Pasquerault).
0379-0738/$ – see front matter # 2003 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/j.forsciint.2003.10.014
76
F. Lefebvre, T. Pasquerault / Forensic Science International 139 (2004) 75–79
plete development were calculated for both species. The total accumulated degree-days needed for larval and complete development at one rearing temperature (ADDi) was calculated from the equation: ADDi ¼ n(TiTs); n is the number of development days; Ti the rearing temperature; Ts is the lower development threshold. The thermal constant was calculated for each of the three constant temperatures (for larval and complete development) to obtain the average ADDT ðmean s2 Þ.
Adults were reared at our laboratory in at room temperature (20 2 8C) and under natural photoperiod for 2 years. For each species, 200 adults were kept in a plastic cage (300 mm 500 mm 500 mm) and provided with sugar and water [11,12]. Adults were allowed to oviposit on the surface of fresh beef muscle of uniform quality [12,13]. The meat was observed several times a day. As soon as eggs had been laid, the meat was transferred in a plastic box (260 mm 130 mm 77 mm) containing a layer of sand (30 mm thick) for larval development. These boxes were put in a FIRLABO SPE 140 H incubator. Larval development took place in a relative humidity of between 75 and 95% and a photoperiod of 12:12 h. Three constant temperature regimes were used: 17 1, 24 1 and 30 1 8C. 24 8C is the temperature chosen by the French Forensic Entomology Department to rear specimens collected at the crime scene or the autopsy. The two other temperatures were chosen because they represent the highest and lowest limits of our incubator to allow an accuracy of 1 8C. The eggs were never directly handled. During larval growth and the pupal stage, the specimens were regularly observed (two to three times per day). The first appearance of different development stages (first, second and third larval instars and puparial stage) was noted for O. aenescens. The percentages of time taken by each stage were calculated and the minimum durations of larval and puparial development were determined. The minimum durations of larval and pupal development were also determined for O. capensis. The numbers of breeding (i), the mean (m), the standard deviation (s2) and the modes (M) of the minimum duration of the larval and the total development were determined. Campbell et al. [14], and Grassberger and Reiter [15,16] reported that the development of insects can be described using temperature summation, the accumulation degreedays (ADD) model. It is only valid for the linear portion of the sigmoid development curve. The minimum threshold of development (Ts) for each species was calculated from a linear regression (Microsoft1 Excel 98) of the development rates (t ¼ 1/development time) following the constant temperature: t ¼ f(T8C). Values Ts of the larval and the com-
3. Results 3.1. Ophyra aenescens (Wiedemann, 1830) This species is easily reared in laboratory conditions, a maximum of viable eggs is usually laid on the substrate (beef meat). During the larval growth the duration of the development period decreased as the rearing temperature increased. For each temperature, the minimum duration of the larval development, was measured with six replicates. The total development was measured with 7 replicates at 17 8C, 23 at 24 8C and 11 at 30 8C. For each replicate and rearing temperature regime, the first appearance of the different larval stages, the first puparium and the first adult emergence were noted. The minimum duration at each development stage and the minimum duration of total development at each temperature regime are given in Table 1. The percentage of time taken by each stage is also calculated. The minimum duration of the egg incubation is about 5– 6% of the total development period. The first and second larval stages are sub equal and each of them represents about 10–12% of the total development time. The minimum duration of the puparial stage is as long as the total larval development one. Overall, the duration of the different stages of development decreases as the rearing temperature rises. The average minimum larval and total time of development of this species are presented in Table 2. The minimum duration of larval development is 1.90 times longer at 17 8C
Table 1 Minimum duration of the development stages of O. aenescens (in hours) Stage
17 1 8C
24 1 8C
30 1 8C
First appearance
%
First appearance
%
First appearance
%a
Egg First instars Second instars Third instarsb Pupalc
48 98 88 198 393
6 12 11 24 47
20 46 40 124 168
5 12 10 31 42
14 24 24 80 130
5 9 9 29 48
Total
825
–
398
–
272
–
a
Percentage of total development time. b Post-feeding stage included. c Puparation to emergence.
a
a
F. Lefebvre, T. Pasquerault / Forensic Science International 139 (2004) 75–79
77
Table 2 Average minimum duration of larval and total development of O. aenescens (in days) 17 1 8C
Larval development Total development
24 1 8C 2
30 1 8C 2
M
n
m
s2
M
9 17
11 11
6.6 12.4
0.69 0.74
6 12
n
m
s
M
n
m
s
6 7
18.2 37.1
2.48 4.71
19 nsa
22 23
9.5 17.6
1.46 1.87
n: number of breeding; m: average minimum duration; s2: standard deviation; M: mode. a Missing data.
Fig. 1. Linear regression of the larval and total development of O. aenescens.
than at 24 8C, 2.77 times longer at 17 8C than at 30 8C and 1.45 times longer at 24 8C than at 30 8C. The minimum duration of a complete cycle is 2.11 times longer at 17 8C than at 24 8C, 2.99 times longer at 17 8C than at 30 8C and 1.42 times longer at 24 8C than at 30 8C. The relationship between the development rate of O. aenescens and rearing temperature is shown in Fig. 1. Larval development rates are 0.06, 0.11 and 0.15, respectively at 17, 24 and 30 8C. The equation of the regression line is y ¼ 0:0069x 0:0573 ðR2 ¼ 0:9996Þ where y is the development rate and x is the rearing temperature. The minimum threshold Ts for the larval development is 8.3 8C and the thermal constant ADDL is 149:90 7:98 degree-days above Ts. Total development rates are 0.03, 0.06 and 0.08, respectively at 17, 24 and 30 8C. The linear regression of development rate from egg to adult is y ¼ 0:0039x 0:0346 ðR2 ¼ 0:995Þ. The minimum threshold Ts for the total development is 8.9 8C and the thermal constant ADDT is 276:10 21:50 degree-days above Ts. 3.2. Ophyra capensis (Wiedemann, 1818) Compared with O. aenescens, the duration of development is shortened when the constant rearing temperature is higher but the mortality is more important that of O. aenescens (unpublished data). That is the reason why, during the experiments, disturbance was kept to a minimum. The duration of each larval stage was not studied in this species. To determine the minimum duration of the larval development, 11 replicates were run at 17 8C, 19 at 24 8C and 18 at
30 8C. For the minimum duration of the total development, 8 replicates were run at 17 8C, 19 at 24 8C and 16 at 30 8C. The minimum larval and total time of development of this species are given in Table 3. The minimum duration of larval development is 2.86 times longer at 17 8C than at 24 8C, 5.42 times longer at 17 8C than at 30 8C and 1.89 times longer at 24 8C than at 30 8C. The minimum duration of a complete cycle is 2.95 times longer at 17 8C than at 24 8C, 4.96 times longer at 17 8C than at 30 8C and 1.68 times longer at 24 8C than at 30 8C. The development rates of O. capensis, at different experimental temperatures, are shown in Fig. 2. The larval development rates are 0.03, 0.08 and 0.14, respectively at 17, 24 and 30 8C. The equation of the regression line is y ¼ 0:0084x 0:1161 ðR2 ¼ 0:9907Þ where y is the development rate and x is the rearing temperature. The minimum threshold Ts for the larval development is 13.8 8C and the thermal constant ADDL is 123:32 11:06 degree-days above Ts. The rates of total regression are 0.02, 0.05 and 0.08, respectively at 17 1, 24 1 and 30 1 8C. The linear regression of development rate from egg to adult is y ¼ 0:0046x 0:059 ðR2 ¼ 0:998Þ. The minimum threshold Ts of total development is 12.8 8C and the thermal constant ADDT is 237:05 22:73 degree-days above Ts.
4. Discussion Species of ‘‘dump flies’’, such as O. aenescens, are often used as a biological control agent of the house fly Musca
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Table 3 Average minimum duration of larval and total development of O. capensis (in days) 17 1 8C
Larval development Total development
24 1 8C 2
30 1 8C 2
M
n
m
s2
M
12 21
18 16
7.0 12.5
0.77 0.82
7 13
n
m
s
M
n
m
s
11 8
37.9 62.0
4.53 5.53
34 nsa
19 19
13.3 21.1
1.28 2.01
n: number of breeding; m: average minimum duration; s2: standard deviation; M: mode. a Missing data.
Fig. 2. Linear regression of the larval and total development of O. capensis.
domestica Linneaus, 1758 in poultry houses. Their biology and behaviour are well documented. Johnson and Venard have shown that O. aenescens has a generation time of 14 days at 26:5 1 8C [17]. In contrast, Schuman has reported that the same cycle ended in 8 days at 23 8C [18]. Our study shows that complete development of O. aenescens takes 17:6 1:87 days at 24 8C. Using the thermal development model, the durations of the total development of this species were estimated in 19:6 1:5 days at 23 8C and in 15:7 1:2 days at 26.5 8C. These results are similar to those obtained by Johnson and Venard but they differ greatly of those reported by Schuman. In both cases however, some differences in the development times remain. The development of insects depends on numerous factors including the experimental conditions of rearing. The variation of the photoperiod or relative humidity or larval development substrate could explain the different duration of development times observed. The geographic origin of the populations could be considered as another factor that may also partly explain these differences. Grassberger and Reiter [15,16], and Greenberg [19] assumed that the fly necrophagous species presented geographic variation and adaptation. Their development times may differ under the same environmental conditions according to the population studied. Likewise, under the same rearing conditions, the duration of the larval development of O. capensis could be longer that of O. aenescens. For O. aenescens, the percentage of duration of the larval development is 50%. It is 60% for O. capensis. The development threshold Ts of O. capensis is higher than the Ts of O. aenescens. These results suggest that
O. capensis requires milder temperature conditions to develop properly as O. aenescens. They also show that the optimal development temperature of O. capensis is higher than O. aenescens one [6]. Little data is known about O. capensis and in particular its biology is poorly documented. However, they are important for forensic entomology because these species may be associated with human cadavers. O. capensis is frequently identified by our unit; 10% of the cases studied since 1992 [20] contain that species.
5. Conclusion The temperature-dependent development models of O. aenescens and O. capensis are determined for rearing temperature included between 17 and 30 8C corresponding to the linear sections of the sigmoid development curve models for these species. These experiments were carried out in constant temperatures. In forensic entomology, this situation is similar to an indoor crime scene. Outdoors, the quality of the temperature records will be important in allowing these data to be of value in the Post-Mortem Interval investigation.
Acknowledgements We thank very much Benoıˆt Vincent and Emmanuel Carcreff for their great help to carry out these experiments. We thank also Emmanuel Gaudry, Laurent Dourel, Bernard Chauvet and Jean-Bernard Myskowiak for their constant
F. Lefebvre, T. Pasquerault / Forensic Science International 139 (2004) 75–79
assistance. Special thanks to Bryan Turner for his great help. Lastly, we are very grateful to Yvan Malgorn and Frederic Brard for their precious advices.
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