- Email: [email protected]
Unidirectional en masse larval dispersal of blow flies (Diptera: Calliphoridae)
Journal Pre-proof Unidirectional en masse larval dispersal of blow flies (Diptera: Calliphoridae)
Jerome Goddard, Grant De Jong, Florencia Meyer PII:
S2352-2496(19)30055-2
DOI:
https://doi.org/10.1016/j.fooweb.2019.e00137
Reference:
FOOWEB 137
To appear in:
Food Webs
Received date:
1 November 2019
Revised date:
11 December 2019
Accepted date:
21 December 2019
Please cite this article as: J. Goddard, G. De Jong and F. Meyer, Unidirectional en masse larval dispersal of blow flies (Diptera: Calliphoridae), Food Webs(2020), https://doi.org/ 10.1016/j.fooweb.2019.e00137
This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
© 2020 Published by Elsevier.
Journal Pre-proof
SHORT COMMUNICATION
ro
of
Unidirectional En Masse Larval Dispersal of Blow Flies (Diptera: Calliphoridae) Jerome Goddard,1,2 Grant De Jong,1 and Florencia Meyer1
ur
na
lP
Corresponding author (Email: [email protected]).
Jo
2
re
-p
Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology Box 9775, Mississippi State, MS 39762 USA
1
Journal Pre-proof Abstract Decomposition of carrion is a complex ecological process wherein nutrients and energy are recycled in the environment. After feeding but prior to pupation, blow fly larvae disperse from decomposing carrion, presumably to escape unfavorable microsite conditions or perhaps predation. By leaving the immediate area, larvae are effectively transporting carrion-derived nutrients throughout the ecosystem. This dispersal is generally characterized as individual-based
of
and moving randomly from the carcass in every direction, however, non-random, en masse
ro
maggot dispersal has been documented at least twice. Here we report another incidence of en
-p
masse blow fly larval dispersal traveling due east in a small column. At approximately 2 m, the
re
column stopped its unidirectional path and dispersed in a radial, 3600 pattern. A subsample of 5 larvae was collected, returned to the lab, and identified as Lucilia coeruleiviridis, a common
lP
blow fly often involved in carrion decomposition in nature. These observations contribute to an
na
increasing body of evidence that migrating fly larvae do not always disperse randomly, which may have important implications for the dispersal of carrion-derived nutrients as well as
Jo
ur
interactions with blow fly predators.
Keywords: Forensic entomology; Necrobiome; Invertebrate scavengers; Decomposition; Lucilia coeruliviridis
2
Journal Pre-proof Decomposition of corpses and carrion disperses energy and nutrients concentrated by living organisms back into the environment (Barton et al. 2019), and community assembly – such as that associated with decaying carrion – often exhibits particular ecological patterns which can be studied and predicted (Vanlaerhoven 2010). Globally, vertebrate scavengers such as vultures are among the most persecuted and imperiled species (Buechley and Sekercioglu 2016), which may contribute to increasing importance of invertebrates in the decomposition
of
process as predicted with other aspects of global change (Tomberlin et al. 2017, Olea et al.
ro
2019). Knowledge of blow fly species and their behavior in a given area are important to
-p
ecologists, entomologists, and forensic scientists. Several studies have documented blow fly
re
species present in Mississippi, USA and offered comments about their role in the decomposition process (Goddard and Lago 1983, Goddard and Lago 1985, Goddard et al. 2012). In nature,
lP
carrion is visited by blow flies almost immediately after death, which lay their eggs in natural
na
orifices or tears/openings in the flesh. Blow fly larvae then feed on the decaying tissue through three larval stages, after which the post-feeding third instar blow fly larvae begin dispersal to
ur
pupate. In general, these larvae move away from the carcass 5-10 meters and pupate at the soil
Jo
surface (rarely just below).
Blow fly larval dispersal is generally individual-based and random in every direction (Smith et al. 1981, Byrd and Castner 2010). However, since 2011, there have been two reports of massive and synchronized dispersal of blow fly larvae from decaying pigs. One was during a mass mortality study in Mississippi, USA using 725kg/20m2 of carrion and the other utilized 6 replicates of 14-18 kg pigs in Ohio (Lewis and Benbow 2011, Lashley et al. 2018) (Table 1). Because blow fly larvae grow and develop by consuming carrion nutrients, previous authors have speculated that their dispersal from carcass sites has important ecosystem implications,
3
Journal Pre-proof however, dispersal in general, and particularly this phenomenon of “group” dispersal, is not welldocumented or studied enough to make educated guesses as to its significance. Here we report a third incidence of en masse blow fly larval dispersal. These observations contribute to a growing body of evidence that dispersing fly larvae do not always disperse randomly, raising questions about the benefits and costs of synchronized dispersal, as well as its impacts on predation and nutrient flow away from carcasses.
of
Our study consisted of 3 domestic swine (Sus scrofa), approximately 3 kg each, placed in
ro
a rural meadow near Adaton, MS, USA and observed daily for 10 days. We replicated this
-p
design 4 times, observing 12 carcasses in total. In each replicate, carcasses were placed
re
approximately 2-4 m from each other. Land surrounding the cages was almost entirely flat with
lP
recently mowed grass (< 5 cm tall). The experiment was conducted to evaluate the effects of fire ants on carrion decomposition. Thus, each carcass was enclosed in a fabric bag of different
na
size “mesh” to exclude colonizers of different body sizes.
ur
Based on our observations, all swine carcasses displayed previously described decomposition patterns, fly and other invertebrate scavenger activity, and random blow fly larval
Jo
dispersal. However, on day 7, approximately 8:00 am, a distinct column of blow fly larvae was observed dispersing from the control pig. The column (approx. 12.5 cm wide and 1.37 m long) consisted of hundreds of post-feeding third instar larvae traveling due east at 5.1 cm/min. A piece of paper was placed in front of the advancing column to facilitate photography and the larvae subsequently attempted to cross it as well (Figure 1). At approximately 2 m from the carcass, the column stopped its unidirectional path and larvae dispersed in a radial, 3600 pattern. A subsample of 5 larvae was collected, returned to the lab, and identified as Lucilia
4
Journal Pre-proof coeruleiviridis, a common blow fly in Mississippi known to be involved in decomposition of carrion (Goddard and Lago 1983). This mass migration event was unusual in that we repeated our pig decay experiment 4 times (3 pigs each time), and of the 12 replicates, only once did we observe unidirectional mass maggot migration. However, our observations only occurred for 3 hours per day, therefore there is a possibility we missed mass migrations at the other 11 carcasses. As for relevance of these
of
findings, Lewis and Benbow (2011) discussed the forensic implications, and Lashley et al (2018)
ro
speculated on the indirect effects of mass migration in ecosystems. Here we offer ideas on the
-p
biological significance of the phenomenon. Ecological factors explaining why larvae engage in
re
this en masse behavior remain largely unknown, but there are several possibilities:
lP
1. Traveling en masse may facilitate longer dispersal of each individual.
na
2. Larvae may be escaping microsite characteristics that deter successful pupation and (subsequent) emergence as adult flies. This may include saturated soil from carrion
ur
fluids, toxic conditions, and geological characteristics.
Jo
3. Moving away from carrion may help larvae escape high pathogen densities at the decomposition site. 4. Traveling en masse may aid individual thermoregulation. 5. Larvae may be escaping areas of higher predation. However, one study showed that insectivores (nine-banded Armadillo, Dasypus novemcinctus) followed the path of larvae, presumable digging up and consuming pupae in the soil (Lashley et al. 2018). Therefore, dispersing away from carcasses certainly does not offer complete reprieve from predators.
5
Journal Pre-proof
Further research concerning blow fly en masse larval migration is needed, perhaps using round-the-clock time-lapse photography, to carefully document dispersal patterns, to confirm how frequently such events occur, and to explore potential causes and adaptive significance of this behavior.
of
Acknowledgments
re
-p
ro
Catherine Gibson and Brooklyn Thompson helped with this study.
Jo
ur
na
lP
Table 1. Characteristics of mass larval dispersal. Study Carrion Species Size and size/amount involved shape of mass Lashley Multiple Not identified1 Broad, et al. feral swine, several 2018 725 kg/20m2 meters wide Lewis 6 pigs Phormia Columnar, and (individually regina 0.36 m Benbow placed) 14wide3 2011 18 kg each Current Pig, approx. Lucilia Narrow 4 study 3 kg coeruleiviridis column, 0.127 m
1
Depth of mass >5 cm
1-6 cm
5 cm
Speeds and direction of travel Followed topography (downhill),1 speed not given 2.7 cm/min, North/northeast
5.1 cm/min Due East
Length of dispersal 20-50 m2
Up to 26 m
2.13 m
Larvae not identified, but adults collected at the site included Cochiomyia macellaria and Phormia regina. 2 Estimated (personal communication with authors), not reported in their paper. 3 Several migrating masses observed. Apparently, only one mass carefully measured. 4 Subsample of larval mass were identified as this species. In addition, pitfall traps samples of larvae from the same date and pig were also only Lucilia coeruleiviridis.
6
Journal Pre-proof
Jo
References
ur
na
lP
re
-p
ro
of
Figure 1. Mass dispersal of blow fly larvae.
Barton, P. S., M. J. Evans, C. N. Foster, J. L. Pechat, J. K. Bump, M. M. Quaggiotto, and M. E. Benbow. 2019. Towards quantifying carrion biomass in ecosystems. Trends Ecol. Evol. 34: 950-961. Buechley, E. R., and C. H. Sekercioglu. 2016. The avian scavenger crisis: looming extinctions, trophic cascades, and loss of critical ecosystems. Biol. Conserv. 198: 220-228. Byrd, J. H., and J. L. Castner. 2010. Insects of forensic importance, pp. 39-126. In J. H. Byrd and J. L. Castner (eds.), Forensic Entomology: The Utility of Arthropods in Legal Investigations. CRC Press, Boca Raton, FL. Goddard, J., and P. K. Lago. 1983. An annotated list of the Calliphoridae of Mississippi. J. Georgia Entomol. Soc. 18: 481-484. Goddard, J., and P. K. Lago. 1985. Notes on blow fly succession on carrion in northern Mississippi. J. Entomol. Sci. 20: 312-317.
7
Journal Pre-proof
Jo
ur
na
lP
re
-p
ro
of
Goddard, J., D. Fleming, J. L. Seltzer, S. Anderson, C. Chesnut, M. Cook, E. L. Davis, B. Lyle, S. Miller, E. A. Sansevere, and W. Schubert. 2012. Insect succession on pig carrion in north-central Mississippi. Midsouth Entomol. 5: 39-53. Lashley, M. A., H. R. Jordan, J. K. Tomberlin, and B. T. Barton. 2018. Indirect effects of larval dispersal following mass mortality events. Ecology 99: 491-493. Lewis, A. J., and M. E. Benbow. 2011. When entomological evidence crawls away: Phormia regina en masse larval dispersal. J. Med. Entomol. 48: 1112-1119. Olea, P. P., P. Mateo-Tomas, and P. S. Barton. 2019. Invertebrate scavengers matter. Science 363: 1162. Smith, R. H., R. Dallwitz, K. G. Wardhaugh, W. G. Vogt, and T. L. Woodburn. 1981. Timing of larval exodus from sheep and carrion in the sheep blowfly, Lucilia cuprina. Entomol. Exp. Appl. 30: 157-162. Tomberlin, J. K., B. T. Barton, and M. A. Lashley. 2017. Mass mortality events and the role of necrophagous invertebrates. Curr. Opin. Insect Sci. 23: 7-12. Vanlaerhoven, S. L. 2010. Ecological theory and its application in forensic entomology, pp. 493-517. In J. H. Byrd and J. L. Castner (eds.), Forensic Entomology: The Utility of Arthropods in Legal Investigations. CRC Press, Boca Raton, FL.
8
Jerome Goddard, Grant De Jong, Florencia Meyer PII:
S2352-2496(19)30055-2
DOI:
https://doi.org/10.1016/j.fooweb.2019.e00137
Reference:
FOOWEB 137
To appear in:
Food Webs
Received date:
1 November 2019
Revised date:
11 December 2019
Accepted date:
21 December 2019
Please cite this article as: J. Goddard, G. De Jong and F. Meyer, Unidirectional en masse larval dispersal of blow flies (Diptera: Calliphoridae), Food Webs(2020), https://doi.org/ 10.1016/j.fooweb.2019.e00137
This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.
© 2020 Published by Elsevier.
Journal Pre-proof
SHORT COMMUNICATION
ro
of
Unidirectional En Masse Larval Dispersal of Blow Flies (Diptera: Calliphoridae) Jerome Goddard,1,2 Grant De Jong,1 and Florencia Meyer1
ur
na
lP
Corresponding author (Email: [email protected]).
Jo
2
re
-p
Department of Biochemistry, Molecular Biology, Entomology and Plant Pathology Box 9775, Mississippi State, MS 39762 USA
1
Journal Pre-proof Abstract Decomposition of carrion is a complex ecological process wherein nutrients and energy are recycled in the environment. After feeding but prior to pupation, blow fly larvae disperse from decomposing carrion, presumably to escape unfavorable microsite conditions or perhaps predation. By leaving the immediate area, larvae are effectively transporting carrion-derived nutrients throughout the ecosystem. This dispersal is generally characterized as individual-based
of
and moving randomly from the carcass in every direction, however, non-random, en masse
ro
maggot dispersal has been documented at least twice. Here we report another incidence of en
-p
masse blow fly larval dispersal traveling due east in a small column. At approximately 2 m, the
re
column stopped its unidirectional path and dispersed in a radial, 3600 pattern. A subsample of 5 larvae was collected, returned to the lab, and identified as Lucilia coeruleiviridis, a common
lP
blow fly often involved in carrion decomposition in nature. These observations contribute to an
na
increasing body of evidence that migrating fly larvae do not always disperse randomly, which may have important implications for the dispersal of carrion-derived nutrients as well as
Jo
ur
interactions with blow fly predators.
Keywords: Forensic entomology; Necrobiome; Invertebrate scavengers; Decomposition; Lucilia coeruliviridis
2
Journal Pre-proof Decomposition of corpses and carrion disperses energy and nutrients concentrated by living organisms back into the environment (Barton et al. 2019), and community assembly – such as that associated with decaying carrion – often exhibits particular ecological patterns which can be studied and predicted (Vanlaerhoven 2010). Globally, vertebrate scavengers such as vultures are among the most persecuted and imperiled species (Buechley and Sekercioglu 2016), which may contribute to increasing importance of invertebrates in the decomposition
of
process as predicted with other aspects of global change (Tomberlin et al. 2017, Olea et al.
ro
2019). Knowledge of blow fly species and their behavior in a given area are important to
-p
ecologists, entomologists, and forensic scientists. Several studies have documented blow fly
re
species present in Mississippi, USA and offered comments about their role in the decomposition process (Goddard and Lago 1983, Goddard and Lago 1985, Goddard et al. 2012). In nature,
lP
carrion is visited by blow flies almost immediately after death, which lay their eggs in natural
na
orifices or tears/openings in the flesh. Blow fly larvae then feed on the decaying tissue through three larval stages, after which the post-feeding third instar blow fly larvae begin dispersal to
ur
pupate. In general, these larvae move away from the carcass 5-10 meters and pupate at the soil
Jo
surface (rarely just below).
Blow fly larval dispersal is generally individual-based and random in every direction (Smith et al. 1981, Byrd and Castner 2010). However, since 2011, there have been two reports of massive and synchronized dispersal of blow fly larvae from decaying pigs. One was during a mass mortality study in Mississippi, USA using 725kg/20m2 of carrion and the other utilized 6 replicates of 14-18 kg pigs in Ohio (Lewis and Benbow 2011, Lashley et al. 2018) (Table 1). Because blow fly larvae grow and develop by consuming carrion nutrients, previous authors have speculated that their dispersal from carcass sites has important ecosystem implications,
3
Journal Pre-proof however, dispersal in general, and particularly this phenomenon of “group” dispersal, is not welldocumented or studied enough to make educated guesses as to its significance. Here we report a third incidence of en masse blow fly larval dispersal. These observations contribute to a growing body of evidence that dispersing fly larvae do not always disperse randomly, raising questions about the benefits and costs of synchronized dispersal, as well as its impacts on predation and nutrient flow away from carcasses.
of
Our study consisted of 3 domestic swine (Sus scrofa), approximately 3 kg each, placed in
ro
a rural meadow near Adaton, MS, USA and observed daily for 10 days. We replicated this
-p
design 4 times, observing 12 carcasses in total. In each replicate, carcasses were placed
re
approximately 2-4 m from each other. Land surrounding the cages was almost entirely flat with
lP
recently mowed grass (< 5 cm tall). The experiment was conducted to evaluate the effects of fire ants on carrion decomposition. Thus, each carcass was enclosed in a fabric bag of different
na
size “mesh” to exclude colonizers of different body sizes.
ur
Based on our observations, all swine carcasses displayed previously described decomposition patterns, fly and other invertebrate scavenger activity, and random blow fly larval
Jo
dispersal. However, on day 7, approximately 8:00 am, a distinct column of blow fly larvae was observed dispersing from the control pig. The column (approx. 12.5 cm wide and 1.37 m long) consisted of hundreds of post-feeding third instar larvae traveling due east at 5.1 cm/min. A piece of paper was placed in front of the advancing column to facilitate photography and the larvae subsequently attempted to cross it as well (Figure 1). At approximately 2 m from the carcass, the column stopped its unidirectional path and larvae dispersed in a radial, 3600 pattern. A subsample of 5 larvae was collected, returned to the lab, and identified as Lucilia
4
Journal Pre-proof coeruleiviridis, a common blow fly in Mississippi known to be involved in decomposition of carrion (Goddard and Lago 1983). This mass migration event was unusual in that we repeated our pig decay experiment 4 times (3 pigs each time), and of the 12 replicates, only once did we observe unidirectional mass maggot migration. However, our observations only occurred for 3 hours per day, therefore there is a possibility we missed mass migrations at the other 11 carcasses. As for relevance of these
of
findings, Lewis and Benbow (2011) discussed the forensic implications, and Lashley et al (2018)
ro
speculated on the indirect effects of mass migration in ecosystems. Here we offer ideas on the
-p
biological significance of the phenomenon. Ecological factors explaining why larvae engage in
re
this en masse behavior remain largely unknown, but there are several possibilities:
lP
1. Traveling en masse may facilitate longer dispersal of each individual.
na
2. Larvae may be escaping microsite characteristics that deter successful pupation and (subsequent) emergence as adult flies. This may include saturated soil from carrion
ur
fluids, toxic conditions, and geological characteristics.
Jo
3. Moving away from carrion may help larvae escape high pathogen densities at the decomposition site. 4. Traveling en masse may aid individual thermoregulation. 5. Larvae may be escaping areas of higher predation. However, one study showed that insectivores (nine-banded Armadillo, Dasypus novemcinctus) followed the path of larvae, presumable digging up and consuming pupae in the soil (Lashley et al. 2018). Therefore, dispersing away from carcasses certainly does not offer complete reprieve from predators.
5
Journal Pre-proof
Further research concerning blow fly en masse larval migration is needed, perhaps using round-the-clock time-lapse photography, to carefully document dispersal patterns, to confirm how frequently such events occur, and to explore potential causes and adaptive significance of this behavior.
of
Acknowledgments
re
-p
ro
Catherine Gibson and Brooklyn Thompson helped with this study.
Jo
ur
na
lP
Table 1. Characteristics of mass larval dispersal. Study Carrion Species Size and size/amount involved shape of mass Lashley Multiple Not identified1 Broad, et al. feral swine, several 2018 725 kg/20m2 meters wide Lewis 6 pigs Phormia Columnar, and (individually regina 0.36 m Benbow placed) 14wide3 2011 18 kg each Current Pig, approx. Lucilia Narrow 4 study 3 kg coeruleiviridis column, 0.127 m
1
Depth of mass >5 cm
1-6 cm
5 cm
Speeds and direction of travel Followed topography (downhill),1 speed not given 2.7 cm/min, North/northeast
5.1 cm/min Due East
Length of dispersal 20-50 m2
Up to 26 m
2.13 m
Larvae not identified, but adults collected at the site included Cochiomyia macellaria and Phormia regina. 2 Estimated (personal communication with authors), not reported in their paper. 3 Several migrating masses observed. Apparently, only one mass carefully measured. 4 Subsample of larval mass were identified as this species. In addition, pitfall traps samples of larvae from the same date and pig were also only Lucilia coeruleiviridis.
6
Journal Pre-proof
Jo
References
ur
na
lP
re
-p
ro
of
Figure 1. Mass dispersal of blow fly larvae.
Barton, P. S., M. J. Evans, C. N. Foster, J. L. Pechat, J. K. Bump, M. M. Quaggiotto, and M. E. Benbow. 2019. Towards quantifying carrion biomass in ecosystems. Trends Ecol. Evol. 34: 950-961. Buechley, E. R., and C. H. Sekercioglu. 2016. The avian scavenger crisis: looming extinctions, trophic cascades, and loss of critical ecosystems. Biol. Conserv. 198: 220-228. Byrd, J. H., and J. L. Castner. 2010. Insects of forensic importance, pp. 39-126. In J. H. Byrd and J. L. Castner (eds.), Forensic Entomology: The Utility of Arthropods in Legal Investigations. CRC Press, Boca Raton, FL. Goddard, J., and P. K. Lago. 1983. An annotated list of the Calliphoridae of Mississippi. J. Georgia Entomol. Soc. 18: 481-484. Goddard, J., and P. K. Lago. 1985. Notes on blow fly succession on carrion in northern Mississippi. J. Entomol. Sci. 20: 312-317.
7
Journal Pre-proof
Jo
ur
na
lP
re
-p
ro
of
Goddard, J., D. Fleming, J. L. Seltzer, S. Anderson, C. Chesnut, M. Cook, E. L. Davis, B. Lyle, S. Miller, E. A. Sansevere, and W. Schubert. 2012. Insect succession on pig carrion in north-central Mississippi. Midsouth Entomol. 5: 39-53. Lashley, M. A., H. R. Jordan, J. K. Tomberlin, and B. T. Barton. 2018. Indirect effects of larval dispersal following mass mortality events. Ecology 99: 491-493. Lewis, A. J., and M. E. Benbow. 2011. When entomological evidence crawls away: Phormia regina en masse larval dispersal. J. Med. Entomol. 48: 1112-1119. Olea, P. P., P. Mateo-Tomas, and P. S. Barton. 2019. Invertebrate scavengers matter. Science 363: 1162. Smith, R. H., R. Dallwitz, K. G. Wardhaugh, W. G. Vogt, and T. L. Woodburn. 1981. Timing of larval exodus from sheep and carrion in the sheep blowfly, Lucilia cuprina. Entomol. Exp. Appl. 30: 157-162. Tomberlin, J. K., B. T. Barton, and M. A. Lashley. 2017. Mass mortality events and the role of necrophagous invertebrates. Curr. Opin. Insect Sci. 23: 7-12. Vanlaerhoven, S. L. 2010. Ecological theory and its application in forensic entomology, pp. 493-517. In J. H. Byrd and J. L. Castner (eds.), Forensic Entomology: The Utility of Arthropods in Legal Investigations. CRC Press, Boca Raton, FL.
8