Neotrop Entomol

DOI 10.1007/s13744-017-0540-0

ECOLOGY, BEHAVIOR AND BIONOMICS

Diversity, Daily Flight Activity and Temporal Occurrence

of Necrophagous Diptera Associated with Decomposing
Carcasses in a Semi-Arid Environment

DL OLIVEIRA, SD VASCONCELOS
Insects of Forensic Importance Research Group, Dept of Zoology, Univ Federal de Pernambuco, Recife, PE, Brasil

Keywords Abstract
Caatinga, decomposition, blow flies, flesh The harsh conditions of the Brazilian seasonally dry tropical forest known
flies, forensic entomology as Caatinga pose challenges to the insects specialized in the exploitation of
Correspondence ephemeral resources. We investigated the diversity and daily flight activity
Insects of Forensic Importance Research of dipterans associated with decomposing rat carcasses in a field experi-
Group, Universidade Federal de ment performed in the semi-arid region of Pernambuco State, Brazil. We
Pernambuco, Av. Prof. Moraes Rego,
Recife - PE, 50.670-420, Brazil; also analyzed the temporal arrival of adult insects on the carcasses at three
[email protected] stages of decomposition: early, intermediate, and advanced. We collected
1173 individuals, of which Muscidae had the highest abundance (36.5%),
Edited by Patrícia J Thyssen – UNICAMP followed by Sarcophagidae (28.1%), Calliphoridae (25.2%), and Fanniidae
Received 16 March 2017 and accepted 30 (10.2%). Chrysomya albiceps (Wiedemann, 1819) (Calliphoridae), Fannia
June 2017 pusio (Wiedemann, 1830) (Fanniidae), Atherigona orientalis (Schiner,
1868), and Musca domestica (Linnaeus, 1758) (Muscidae) were the most
* Sociedade Entomológica do Brasil 2017
abundant species. The richness reached its maximum value on the second
day of decomposition, with 18 species, decreasing to 8 species on the last
day of decomposition (7 days). The ecological indices of diversity, domi-
nance, and evenness varied little among the stages. There was an overlap
of most species throughout the decomposition, although the overall abun-
dance was higher at the intermediate stage for Calliphoridae, Muscidae,
and Sarcophagidae. In accordance to previous studies, nocturnal flight was
rare, as approximately 8% of insects were captured at night. Our results
expand the knowledge on ecological and behavioral aspects of necropha-
gous flies under inhospitable environments, such as the dry season in the
Caatinga. The dominance of the invasive species C. albiceps reinforced
here illustrates its geographical expansion towards the countryside of
Northeastern Brazil.

Introduction concealed dead animals (Bhadra et al 2014), and reach car-

casses minutes after death in densely forested areas
Necrophagous flies (Diptera) succeed in the colonization of (Vasconcelos et al 2013).
ephemeral resources due largely to their effective response By exploiting ephemeral resources, necrophagous dip-
to visual and olfactory cues (Wall & Fisher 2001). Species of terans developed a unique behavioral repertoire destined
Calliphoridae, Sarcophagidae, Muscidae, and Fanniidae, in to maximize colonization in the shortest temporal scale
particular, seem to excel their competitors in the exploitation (Denno & Cothran 1976, Moura 2004), reducing risks of pre-
of decomposing carcasses and cadavers under unfavorable dation, cannibalism, and exposure to pathogens and parasit-
circumstances. For example, blow flies can locate substrates oids (Amendt et al 2010). Additionally, the ability to reach a
in the absence of light (Aak & Knudsen 2011), detect carcass or cadaver shortly after death is advantageous
 Oliveira & Vasconcelos

because more organic matter is available to the offspring and concentrated from January to May. The mean temperature
fewer competitor species will be present. On an applied lev- varied from 19°C (at night) to 41°C during the day. Vegetation
el, knowledge on pioneer species tends to be useful for the is mostly composed by herbaceous xerophytic and shrub
estimation of the post-mortem interval (PMI) (Catts & Goff species—e.g., Bromelia laciniosa Mart. ex Schult. f.
1992), a key contribution of field-based experiments to fo- (Bromeliaceae), Jatropha sp. (Euphorbiaceae), and Cereus
rensic entomology. jamacaru DC. (Cactaceae), sparsely distributed with numer-
Olfactory cues are mostly represented by volatile organic ous clearings that allow for intense penetration of sunlight.
compounds (VOCs) released by decaying substrates The soil is similar to that described by Silva et al (2009),
(Ashworth & Wall 1994), and the nature and amount of these classified on the sandy class, and with great susceptibility
compounds vary throughout decomposition—thus modify- to erosion. Local vertebrate fauna consists of few goats and
ing the attractiveness to different insect species (Archer & sheep from small-scale livestock, as well as a small number of
Elgar 2003). The decomposition of a substrate is strongly birds and small reptiles.
affected by the carcass size (Sutherland et al 2013) and influ-
enced by local temperature, luminosity, relative air humidity, Insect sampling and identification
rainfall, type of soil, among other biotic and abiotic factors
(Amendt et al 2010). Under inhospitable conditions, such as Rat (Rattus norvegicus) carcasses (Berkenhout, 1769), rang-
excessive temperature and shortage of water, small car- ing from 225 to 287 g (mean 241.8 g± SD 13.7 g), were used as
casses tend to deteriorate fast (Simmons et al 2010). baits. Animals were provided from controlled rearing facili-
Strong competition for declining resources is likely to favor ties and euthanized by exposition to carbon monoxide (CO),
highly competitive species, such as invasive blow flies of the a method recommended by the Brazilian regulation agency
genus Chrysomya (Calliphoridae). for animal experimentation. Previously frozen carcasses were
In the Brazilian seasonally dry tropical forest, known as thawed in individual sealed plastic bags at 24°C for 36 h prior
Caatinga, stressful conditions include irregular rainfall regime to the experiments.
with several months of drought, high temperature and inso- Adult dipterans were collected in traps suspended 1.5 m
lation, and low soil and air moisture (Sampaio 1995). Under a above the soil. Traps consisted on two cylindrical plastic con-
social viewpoint, the Caatinga is the most populous semi-arid tainers (15.0 cm height × 12.5 cm diameter) vertically at-
region in the world, with ca. 27 million inhabitants, and local tached to one another. The carcasses were placed in the
rates of homicide have increased in the past decades lower portion, which had four 3-cm-diameter openings
(Waiselfisz 2016). Hence, behavioral and ecological data on through which insects could access the carcasses. The major-
carcass colonization by necrophagous insects are useful both ity of insects (over 95%, according to pilot tests) flew up-
to diagnose local biodiversity and to strengthen initiatives of wards and got trapped inside the top container (Fig 1a).
forensic entomology in the region. Then, the top container was isolated using a mesh cover
We investigated the diversity of necrophagous Diptera in (Fig 1b) and replaced by a fresh one at each sampling
a fragment of Caatinga under a threefold approach: (i) to timepoint, maintaining the carcasses undisturbed until the
describe the species of four families (Calliphoridae, end of the experiment (Fig 1c).
Fanniidae, Muscidae, and Sarcophagidae) associated with To compare the flight activity, traps remained for 12 ± 1 h
rat carcasses, examining the structure and the composition in the field, to comprise diurnal (from 05h30min to
of assemblages; (ii) to assess for differences in the occur- 17h30min) and nocturnal (from 17h30min to 05h30min) pe-
rence of species at different stages of decomposition; and riods. To minimize flaws related to these treatments, we
(iii) to compare the diurnal and nocturnal flight activity of the waited until dusk and dawn to collect the trapped flies, and
most abundant species. exact time differed slightly according to the month of the
experiment. This process was repeated until the carcasses
were dry, which occurred 7 days after the initial exposure.
Material and Methods All collected insects were identified using the taxonomical
keys of Carvalho et al (2002), Carvalho & Mello-Patiu
Area of study (2008) and Kosmann et al (2013).

The experiment was carried out from May to November Ecological and statistical analysis
2014, in a semi-preserved fragment of Caatinga (65 ha, alti-
tude 340 m) located in the municipality of Tacaratu (08°57′ We characterized the structure and composition of insect
20″S; 38°12′02″W), Pernambuco State, Brazil, distant 336 km assemblages associated with the carcasses taking into con-
from the Atlantic Ocean. Climate is classified as hot semi-arid sideration the richness of species, abundance, diversity
(Köppen’s Bsh), with annual average rainfall of 435 mm (Shannon’s index, H′), evenness (Pielou’s, J), and dominance
Behavioral aspects of necrophagous Diptera in the Caatinga

Fig 1 Representation of the trap used in the experiment. a Complete trap. b Isolation of the flies on top container. c Assemblage of a new trap, with
removal of top container.

(Simpson’s, D). We also analyzed the temporal occurrence of (Fanniidae), Atherigona orientalis (Schiner, 1868), and
species of Calliphoridae, Fanniidae, Muscidae, and Musca domestica (Linnaeus, 1758) (Muscidae) were the most
Sarcophagidae throughout the decomposition. Due to the abundant species and their abundance summed up 63.9% of
fast decomposition of the substrate, three main stages were all individuals. Due to incomplete taxonomical identifications,
defined, based on visual and physical-chemical characteris- female specimens of Sarcophagidae were treated as a single
tics of the carcasses: early, intermediate, and advanced. taxon (Table 1).
Insect abundance at each decomposition stage was com- The number of species varied across decomposition: only
pared by ANOVA or Kruskal-Wallis variance analyses. In order Tricharaea (Sarcophagula) occidua (Fabricius, 1794)
to discriminate the similarity between the phases of decom- (Sarcophagidae) occurred on the first 12 h, while at least 18
position, the raw data matrix was transformed by log (x + 1) species were registered on the second day. From then on,
and in presence/absence matrices for Bray-Curtis similarity the richness of species decreased to only eight species on the
analysis, which subsidized the construction of non-metrics seventh day. Abundance increased dramatically on the sec-
multidimensional scaling (NMDS), later corroborated by ond and third days, reaching its peak on the third day, with
ANOSIM. 22.3% of all individuals. From the fourth day on, the abun-
Further analyses on the effect of decomposition stage on dance gradually decreased until the last day of observation.
insects’ abundance were performed for species with ≥90 The period of decomposition was divided as follows: initial
individuals. Abundance at each period (diurnal vs. nocturnal) stage (days 0 to 2), intermediate (days 3 to 5), and advanced
was compared through Chi square. We used a total of 29 (days 6 and 7). Insect abundance at the days of intermediate
independent replicates (rat carcasses) throughout a 7- stage was significantly greater than that at the other stages
month sampling period. The softwares BioEstat 5.0, Primer (H = 57.02; d.f. = 7; P < 0.0001). The mean distribution of flies
6.0, and SigmaPlot 10.0 were used, considering 5% signifi- along the decomposition followed a normal-like curve (Fig 2).
cance level for all analysis. All procedures were approved by The indices of diversity, dominance, and evenness were
the local Ethics Committee (protocol: 23076.023896/2014- similar between stages. Shannon-Wiener’s diversity index
21) and environmental agencies for biological conservation. ranged from H′ = 1.44 to H′ = 1.92 (mean H′ = 1.76),
Simpson’s dominance varied from D′ = 0.66 to D′ = 0.84
(mean D′ = 0.77) and Pielou’s evenness varied from J′ = 0.61
Results to J′ = 0.83 (mean J′ = 0.72). Because of the different com-
position, the abundance rankings displayed different shapes,
When all samplings were combined, 1173 insects were col- with co-dominance of the species C. albiceps, F. pusio, A.
lected in the following proportions: Calliphoridae (25.2%), orientalis, and M. domestica throughout the experiment
Fanniidae (10.2%), Muscidae (36.5%), and Sarcophagidae (Fig 3a–c).
(28.1%). Chrysomya albiceps (Wiedemann, 1819) The overall abundance was higher in the intermediate
(Calliphoridae), Fannia pusio (Wiedemann, 1830) stage (F2; 84 = 9.31; P = 0.0004), and this pattern was
 Oliveira & Vasconcelos

Table 1 Species associated with

decomposing rat carcasses in the Family/species Stage and day of decomposition
Caatinga, according to the
abundance and stage of Early Intermediate Advanced
decomposition.
0 1 2 3 4 5 6 7
Calliphoridae
Chloroprocta idioidea (Robineau-Desvoidy, 1830) – – – – • – – –
Chrysomya albiceps (Wiedemann, 1819) – •• ••• ••• ••• •• • ••
Chrysomya megacephala (Fabricius, 1794) – – • • • • – –
Chrysomya putoria (Wiedemann, 1818) – – – • • – – –
Cochliomyia macellaria (Fabricius, 1775) – • • • – – • –
Fanniidae
Fannia pusio (Wiedemann, 1830) – – • •• •• •• • •
Fannia yenhedi (Albuquerque, 1957) – – • • • – – –
Fanniidae sp. – – •• •• •• •• • •
Muscidae
Atherigona orientalis (Schiner, 1868) – • •• •• •• ••• •• ••
Musca domestica (Linnaeus, 1758) – • ••• ••• •• •• •• •
Ophyra aenescens (Wiedemann, 1830) – • • • • • – •
Ophyra chalcogaster (Wiedemann, 1824) – – • – – – – –
Synthesiomyia nudiseta (Wulp, 1883) – • • – • – – –
Muscidae sp. – – • • • • • –
Sarcophagidae
Argoravinia rufiventris (Walker, 1849) – • – • – • – –
Blaesoxipha (Gigantotheca) stallengi (Lahille, 1907) – – • • – • – –
Oxysarcodexia thornax (Walker, 1849) – – • – – – – –
Ravinia belforti (Prado & Fonseca, 1932) – – – • • • • •
Titanogrypa (Cucullomyia) larvicida (Lopes, 1935) – – • – – – – –
Tricharaea (Sarcophagula) occidua (Fabricius, • – • • – • – –
1794)
Udamopyga setigena (Enderlein, 1928) – • – – – – – –
Sarcophagidae sp. •• • ••• ••• ••• •• •• ••
Total 326 727 120

Legend: – = 0; • = 1 to 9; •• = 10 to 49; ••• = 50 to 99.

repeated for Calliphoridae (P < 0.05), Muscidae (P < 0.006),

and Sarcophagidae (P < 0.05), whereas the abundance of
Fanniidae differed only between early and intermediate
stages (H = 7.76; d.f. = 2; P = 0.007) (Fig 4). At the specific
level, C. albiceps, F. pusio, A. orientalis, and M. domestica
were also collected in higher numbers at the intermediate
stage.
Bray-Curtis analysis with posterior NMDS evidenced
strong similarity in both the structure (species abundance)
and the composition (species presence/absence) of the as-
semblages along the decomposition (Fig 5). There was little
or no tendency to group formation, even after the addition
of a dummy individual with abundance equal to one in all
samples. This lack of grouping was corroborated by the low
Fig 2 Mean abundance (±SD and 95% confidence interval) of flies values in the similarity analyses (ANOSIM), wherein R
collected on rat carcasses, according to the day of decomposition. (structure) global = 0.050 e R (composition) global = 0.115.
Behavioral aspects of necrophagous Diptera in the Caatinga

Fig 3 Abundance ranking of the species on each decomposition stage, depicting the dominant species. a Early. b Intermediate. c Advanced.

Fig 4 Mean abundance (±SD and 95% confidence interval) of each family according to the stage of decomposition. a Calliphoridae. b Fanniidae. c
Muscidae. d Sarcophagidae.
 Oliveira & Vasconcelos

Fig 5 Non-metrics multidimensional scaling (NMDS) of all sampled flies. a Assemblage structure (abundance). b Assemblage composition (presence/
absence).

Flight activity, evidenced by the abundance of captured Discussion

individuals, was approximately 11 times stronger during the
day when compared to the nocturnal period (χ2 = 833.20; In the Caatinga fragment studied here, the richness of
d.f. = 1; P < 0.0001) (Fig 6). This pattern was observed for all Calliphoridae, Fanniidae, Muscidae, and Sarcophagidae did
families and for the most abundant species (P < 0.0001), not differ markedly from studies using rat carcasses in
irrespectively of the decomposition stage. The proportion rainforest fragments (Moretti et al 2008, Magaña et al
of insects in active flight during the day was 89.1% at the 2009), even though this study was performed in the dry
early stage, 92.2% in the intermediate stage, and 96.7% at (and most stressful) season in the semi-arid region.
the advanced stage. Furthermore, studies carried out on urban environment
Several species were collected only during the day: (Azwandi et al 2013) and savannah (Velásquez 2008,
Chrysomya megacephala (Fabricius, 1794), C. putoria Dupont et al 2011) registered lower richness than that ob-
(Calliphoridae), Ophyra chalcogaster (Wiedemann, served here, pointing out that short-term surveys based on
1824) (Muscidae), Blaesoxipha (Gigantotheca) stallengi small carcasses can register a high number of species despite
(Lahille, 1907), Oxysarcodexia thornax (Walker, 1849), the apparently inhospitable environment represented by the
Ravinia belforti (Prado & Fonseca, 1932), Titanogrypa Caatinga. Rat carcasses offer several advantages for ecolog-
(Cucullomyia) larvicida (Lopes, 1935), and Tricharaea ical studies of necrophagous species, as they are frequently
(Sarcophagula) occidua (Sarcophagidae). Contrarily, discarded in sufficient numbers that allow for sound statisti-
Chloroprocta idioidea (Robineau-Desvoidy, 1830) cal analysis. Small size and fast decomposition also favor their
(Calliphoridae) and Udamopyga setigena (Enderlein, use with minimum logistical constraints.
1928) (Sarcophagidae) were only sampled at night. It is widely reported that blow flies tend to numerically
Not only nocturnal registers were rare but also did dominate necrophagous assemblages irrespective of the
they occur at extremely low abundance for all speci- landscape or substrate (Matuszewski et al 2008, Moretti
mens in all treatments. et al 2008) mostly due to their high biotic potential and

Fig 6 Proportion of flies captured in the diurnal and nocturnal sampling periods. a Calliphoridae. b Fanniidae. c Muscidae. d Sarcophagidae.
Behavioral aspects of necrophagous Diptera in the Caatinga

efficient odor-locating apparatus (Byrd & Castner 2009). cadaveric colonization, such as C. albiceps and M. domestica
Surprisingly, species of Muscidae and Sarcophagidae are (Oliveira & Vasconcelos 2010) which in practice can locate a
proven to be as successful as Calliphoridae in the location corpse at night—when most homicides tend to occur.
of (and arrival to) small carcasses in the Caatinga, irrespective Nonetheless, the ability to oviposit in the absence of light is
of the stage decomposition. Even though the invasive blow questionable (Greenberg 1990) and still needs further field
fly C. albiceps prevailed as the dominant species throughout studies.
the decomposition, it was closely followed by M. domestica, Under a practical standpoint, our data highlight the diver-
A. orientalis, and F. pusio. This co-dominance is not often sity of necrophagous Diptera in the Caatinga and clarify as-
registered in studies of necrophagous dipterans associated pects of the attendance of ephemeral resources. The fact
with decomposing animal carcasses or human cadavers, sug- that several of the species registered here have recognized
gesting yet another uniqueness of the Caatinga. medical and veterinary importance as pathogen vectors and
Regarding the temporal occurrence on carcasses, repre- causal agents of myiasis stimulates studies related to, for
sentatives of three families were collected after 24 h of ex- example, the prevalence of facultative myiasis in goats—
position, in conformity with previous register in several en- the most frequently reared livestock in the region (Barbosa
vironments (Martinez et al 2007, Azwandi et al 2013, & Vasconcelos 2015). Ecological models on biological inva-
Vasconcelos et al 2013). This fact draws attention to behav- sion, competition, and niche can be benefitted with the ev-
ioral aspects of non-calliphorid species, which are neglected idence, provided here, that high diversity and intense activity
in the estimation of the PMI, in comparison to blow flies— of necrophagous insects occurs even in the driest periods of
conventionally regarded as pioneer species. In this context, the year in environments deprived of high input of large
to recognize and investigate species from other families as- vertebrate carcasses. Finally, forensic entomology in the re-
sociated with particular stages of decomposition (especially gion is expected to be strengthened by quantitative, field-
initial) may strengthen forensic studies addressed to the es- generated data.
timation of the PMI. While species of Calliphoridae, such as
C. albiceps, have been frequently used as forensic indicators
(Amendt et al 2010), only recently have fanniids begun to get Acknowledgments We thank Conselho Nacional de Desenvolvimento
Científico e Tecnológico (CNPq) and Coordenação de Aperfeiçoamento
documented as entomological evidence on cadavers in South de Pessoal de Nível Superior (CAPES) for financial support, and the col-
America (Vasconcelos et al 2014). leagues from the Insects of Forensic Importance Research Group for
The order in which adult flies attend a decaying substrate critical comments on the manuscript. We also thank Kenio Lima and
can, in some cases, follow a well-defined order (Matuszewski family for all the support during the field research.
et al 2008), and this successional pattern can be
(theoretically) predicted, once it has been observed and rep-
licated (Michaud & Moreau 2009). In the tropical region, Compliance with Ethical Standards All procedures were approved by
especially under arid and semi-arid climates, resource colo- the local Ethics Committee (protocol: 23076.023896/2014-21) and envi-
nization is often subject to a temporal overlap of species ronmental agencies for biological conservation.
(Vasconcelos et al 2016). This was corroborated here by the
absence of groups associated with decomposition stages in
the NMDS and the “R” results close to zero on the ANOSIM. References
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