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Arthropods associated with carrion in a salt marsh habitat in southeastern Florida.

Forensic entomology is used in criminal cases to estimate the postmortem interval (PMI) of a corpse (Byrd & Castner 2010; Tomberlin et al. 2011). Time of year can influence decomposition times due to environmental temperature and seasonality of arthropod species (Campobasso et al. 2001; Amendt et al. 2007; Anderson 2010; Benbow et al. 2013); thus, it is important to determine arthropod diversity, succession, and spatiotemporal biodiversity in different geographic regions and habitats as such information may be useful in decomposition studies (e.g., Turchetto & Vanin 2001; Ngoen-klan et al. 2011; Mohr & Tomberlin 2014). Knowledge of the occurrence of arthropods and how they respond to different environmental conditions improves estimation of the PMI and can help determine if a carcass was relocated from another region (Byrd et al. 2010). The subtropical climate of southern Florida allows most arthropod species to remain active year round. Blow flies (Diptera: Calliphoridae) are the first to visit a carcass, followed by flesh (Diptera: Sarcophagidae) and house (Diptera: Muscidae) flies (Kreitlow 2010). Female flies use the carcass as an oviposition substrate and larval flies eat the carcass tissues.

There are few studies of arthropods associated with carrion in coastal areas (e.g., Barros de Souza et al. 2008 [Brazil], Bucheli et al. 2009 [Texas]; Chen et al. 2014 [Malaysia]) and no known studies in salt marsh regions of Florida. Hence, the objective of this study was to characterize arthropods visiting small animal carcasses in a salt marsh habitat in southeastern Florida. Arthropod diversity is discussed with regard to season.

Materials and Methods

STUDY SITE

All experiments were conducted at a single study site in an open area approximately 4 m from the edge of tidal brackish water connecting to the Indian River Lagoon; 27[degrees] 35' 1" N, 80[degrees] 22' 0" W. Average daily temperature (ADT) was monitored at the Vero Beach Municipal Airport approximately 10 km from the study site (http://cdo.ncdc.noaa.gov/ qclcd/QCLCD). At extreme high tide, the cage containing carrion could be subject to flooding, although no flooding was reported during the study periods. Land crab (Cardisoma guanhumi LatreilleJ holes were observed near the cage. The area 2 m around the cage was devoid of vegetation growth except for red mangrove (Rhizophora mangle L.) seedlings and black mangrove (Avicennia germinans L.) pneumatophores. The overstory of the lowland area was populated by black and red mangroves. There were almost no understory plants in the lowland area; however, there were many mangrove seedlings. The upland overstory vegetation, ranging 2-4 m from the cage, included live oak (Quercus virginiana Miller) that were small, weathered, and stunted; privet (Forestiera segregate [Jacquin], Krug, & Urban) and juvenile sabal palm (Sabal palmetto [Walter] Lodd. ex Schult. & Schult). Understory vegetation was predominately beautyberry (Callicarpa americana L.) and shiny-leafed wild coffee (Psychotria nervosa Swartz). The upland ground had a dense cover of grassy species such as torpedograss (Panicum repens L.). Signs were posted indicating that a forensic study was in progress.

CARCASSES

We collected opossum (Didelphis virginiana Kerr), raccoon (Procyon lotor L.), coyote (Canis latrans Say), bobcat (Lynx rufus Schreber), and otter (Lutra canadensis Schreber) carcasses from roadside locations within a 30 km radius of the study site. Carcasses were transported to the laboratory, examined, and stored in a -20[degrees]C freezer until used for experiments (Institutional Animal Care and Use Committee Protocol Number 201003749). Only fresh carcasses (collected ca. 1-2 d post-mortem that had not yet entered the bloated stage) with no external wounds were used in this study. Immediately prior to each experiment, the selected carcass was weighed and placed in a cylindrical, heavy, galvanized wire mesh cage (16 gauge, 100 cm diameter, 24 cm height). All carcasses were weighed except for the otter and bobcat. The cage had no wire floor and was secured to the ground with plastic tent stakes. The top had a hinged wire mesh door equal to one half the diameter of the cage. The door provided access for sample collecting and was locked to prevent wildlife from disturbing the carcass. Carcasses were placed in the field as shown in Table 1.

OBSERVATIONS AND ARTHROPOD COLLECTIONS

The cage and carcass status was checked daily for the duration of each experiment. Arthropod collections were conducted for ca. 30-45 min. each day using forceps (immature), sweep nets, and mechanical aspirators (adults). No passive trapping methods were used in the current study. Immature and soft-bodied adult arthropods were preserved in 70% ethanol, and other adult arthropods were frozen and pinned. Immature (Stehr 1991; Wells et al. 1999; Byrd & Castner 2010) and adult (Hall 1948; Hall & Townsend 1977; Whitworth 2006) arthropods were identified with taxonomic keys and pictorial keys provided by the Centers for Disease Control and Prevention (http://www.cdc. gov/nceh/ehs/Docs/Pictorial_Keys/Flies.pdf). Because carcass types were not replicated between seasons in this pilot study, only numerical tabulations are reported.

Results

The arthropod species found on respective carcasses are shown in Figs. 1-5 and Table 2. To monitor seasonal presence/absence of arthropods, at least one carcass was placed in the field each season: otter and bobcat (Fall 2009; unknown weights), coyote (Winter 2009, 8.02 kg), raccoon (Spring 2010, 5.22 kg; Fall 2010, 6.37 kg), and opossum (Summer 2010, 4.99 kg). We collected 2,324 specimens from four arthropod orders (Blattodea, Coleoptera, Diptera, and Hymenoptera), including 23 families, 28 genera, and 24 species (Figs. 1-5, Table 2). Specimens were most frequently encountered from Diptera (85% of total), Hymenoptera (8.9%), Coleoptera (1.5%), and Blattodea (0.1%). A total of 1,820 immature and 157 adult Diptera were collected with the majority of collections occurring on the spring (N > 700) and fall (N > 500) raccoon carcasses.

Carcasses were left in the field through all decomposition stages, i.e., fresh to dry remains. Most of the specimens collected were dipteran. Dipterans were collected most frequently from the raccoon carcass (spring; N = 645 larvae, 63 adults) and were observed least frequently from the coyote carcass (winter; N = 72 larvae, 34 adults) (Figs. 1-5, Table 2). Chrysomya rufifacies (Macquart) (Diptera: Calliphoridae) and Musca domestica (L.) (Diptera: Muscidae) represented 50% of dipteran specimens collected. Chrysomya rufifacies was collected more than any other dipteran and the diversity of species collected varied between carcasses. Musca domestica was abundant in spring while C. rufifacies was prevalent in summer and fall. In winter collections, we collected both C. rufifacies and Phormia regina (Meigen) (Diptera: Calliphoridae). Solenopsis invicta (Buren) was collected in every season. Other Hymenoptera (Sphecidae, Vespidae, and/or Chalcididae) were only collected from carcasses in the winter (coyote) and fall (otter and bobcat). Specimens from five families of beetles were collected from the coyote carcass (winter), including Staphylinidae and Dermestidae that are known to be of forensic importance.

Discussion

As expected, longer decomposition times were observed during cooler (e.g., coyote in winter; 46 days) compared with warmer (e.g., opossum in summer; 9 days) periods. A study conducted in southern Ohio placed swine carcasses (14-18 kg) in the field and showed significant seasonal differences in abundance of specimens from Calliphoridae (i.e., P regina and Lucilia coeruleiviridis [Macquart]), Muscidae, Staphylinidae, and Silphidae (Benbow et al. 2013). The weight range (ca. 5-8 kg) of the carcasses used in the current study was similar and likely did not play a major role in species diversity; however, caution is advised when comparing results from similar arthropod succession studies using larger carcasses, as different blow fly species may be attracted to different sized carcasses. Due to the nature of the study's use of carcasses from the roadside, time of death is estimated (fresh carcasses collected 1-2 days post-mortem) and this could impact the PMI.

We observed differences in seasonal distribution (i.e., numbers and species) of dipteran specimens with the highest number collected from the spring raccoon carcass in the field for 24 d. Chrysomya rufifacies, the hairy maggot blow fly, was the species collected most frequently in the current study. Chrysomya rufifaces larvae are predators of other immature dipterans and are known to suppress and/or eliminate other arthropods on carrion when food is scarce (Cammack & Nelder 2010), thereby potentially affecting estimation of the PMI. In another study in Gainesville in north central Florida, C. rufifaces was found to be the dominant species colonizing black bear carcasses, and outcompeting or preying on other arthropods, i.e., C. megacephala (Fabricus), C. macellaria (Fabricus), Lucilia coeruleiviridis (Macquart), P regina, and L. sericata (Meigen) (Swiger et al. 2014). A study conducted near Earleton in northern Florida showed that L. coeruleiviridis was the most prevalent species of Calliphoridae on 16-30 kg pig carcasses (Gruner et al. 2007). A study on blow flies attracted to 60-80 kg pig carcasses in Texas showed C. macellaria and C. rufifaces collected frequently in summer (< 38.2[degrees]C), while C. vicina and P regina were collected most often in the winter (Mohr & Tomberlin 2014). In the current study in a salt marsh environment in southeastern Florida, L. coeruleiviridis was collected in each season, but was most prevalent in spring and fall. We observed P regina most frequently in winter collections in Florida, similar to observations in West Virginia where this species was col lected most frequently in spring (Joy et al. 2002), i.e., average winter temperatures in Vero Beach, Florida are similar to spring temperatures in West Virginia. A study in northern Florida showed P. regina was also most prevalent in winter (Gruner et al. 2007).

Musca domestica was collected in most seasons and was most abundant on the spring raccoon carcass, compared to other carcasses (Fig. 3). A study in northern Thailand showed similar results with most M. domestica collected from traps baited with beef during April-June, although most specimens collected in the aforementioned study were C. megacephala (Ngoen-klan et al. 2011). Musca domestica was considered forensically important on pig carcasses in Argentina (summer, fall, and spring) (Horenstein et al. 2010) and monkey and pig carcasses (summer) in coastal areas of Malaysia (Chin et al. 2008; Chen et al. 2010). Regional temperature differences should be considered when comparing studies where seasonal differences in collections are observed. The low numbers (N = 35) of specimens from order Coleoptera collected were likely due to our collection methods used, which were not effective for this group. Pitfall traps and/or other passive surveillance methods might be better for future studies. Solenopsis invicta were collected for the duration of the study and, since ants are known to eat larval and adult flies and beetles (Campobasso et al. 2009), may have impacted decomposition rates on the carcasses used in the current study. Omnivorous Florida land crabs in the study area are known to eat insects and carrion (Hill 2001); however, this was not directly observed in the current study.

Others have shown no difference in blow fly and beetle activity between pig carcasses frozen (for two months)-thawed and carcasses that were only refrigerated (Bugajski et al. 2011); however, the pig carcasses used in the aforementioned study were smaller (ca. 1 kg) than the carcasses used here. Another study showed anaerobic decomposition in freshly killed rats (ca. 0.316 kg), while aerobic decomposition was predominant in frozen-thawed rats (Micozzi 1986). Further studies should evaluate the effects of freezing on decomposition in different sized carcasses.

This is, to our knowledge, the first report of arthropods associated with carrion from a salt marsh habitat in southeastern Florida. Further studies are needed to characterize arthropods, including the extent to which ecological differences exist between species found in coastal environments. Biodiversity of arthropods in the salt marsh environment is likely affected by environmental factors and this must also be considered in future studies and forensic investigations.

Acknowledgments

The authors acknowledge the helpful contributions of Gregg Ross, Carol Thomas, and Trey English. We thank three reviewers who provided valuable comments that improved the manuscript.

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Stephanie L. Richards (1,2),*, C. Roxanne Connelly (1), Jonathan F. Day (1), Timothy Hope (1), and Ricardo Ortiz (1)

(1) University of Florida, Department of Entomology and Nematology, Florida Medical Entomology Laboratory, Vero Beach, Florida, 32968 USA

(2) Current address: East Carolina University, Department of Health Education and Promotion, Environmental Health Science, Greenville, NC, USA

* Corresponding author; E-mail: richardss@ecu.edu

Caption: Fig. 1. Arthropod diversity (immature and adult) on bobcat and otter during fall 2009.

Caption: Fig. 2. Arthropod diversity (immature and adult) on coyote during winter 2009.

Caption: Fig. 3. Arthropod diversity (immature and adult) on raccoon during spring 2010.

Caption: Fig. 4. Arthropod diversity (immature and adult) on opossum during summer 2010.

Caption: Fig. 5. Arthropod diversity (immature and adult) on raccoon during fall 2010.

Table 1. Description of carcasses placed in the field.

Carcass            Dates                   Days   Average daily
                                                  temperature
                                                  ([degrees]C)

Otter (fall)       September 15-25, 2009   11     27
Bobcat (fall)      October 13-26, 2009     14     28
Coyote (winter)    December 22, 2009-      46     14
                     February 5, 2010
Racoon (spring)    April 12, 2010          24     23
Racoon (fall)      November 10-24, 2010    15     29
Opossum (summer)   July 18-26, 2010        9      29

Table 2. Taxonomic list of arthropod collections by carcass
type, season, and days observed post-placement.

Order         Family          Genus and Species         Days Post
                                                        -placement

Fall 2009--Otter

Diptera       Sarcophagidae   Sarcophaga spp.           1
Diptera       Calliphoridae   Lucilia coeruleiviridis   1
Diptera       Piophilidae     Piophila casei            2
Diptera       Sepsidae        Sepsis spp.               2
Diptera       Ulidiidae       Chaetopsis spp. **        2
Diptera       Calliphoridae   Chrysomya megacephala     2
Diptera       Calliphoridae   Chrysomya rufifacies      2,8
Diptera       Muscidae        Musca domestica           2
Diptera       Calliphoridae   Phormia regina            2
Diptera       Muscidae        Hydrotaea leucostoma      4
Diptera       Stratiomyidae   Hermetia illucens         8
Diptera       Fanniidae       Fannia spp.               11

Fall 2009--Bobcat

Hymenoptera   Formicidae      Solenopsis invicta        1,4,14
Diptera       Muscidae        Hydrotaea leucostoma      3
Hymenoptera   Vespidae        Vespula maculifrons       3
Diptera       Sarcophagidae   Sarcophaga spp.           3
Diptera       Calliphoridae   Phormia regina            3
Diptera       Calliphoridae   Chrysomya rufifacies      3,4
Diptera       Calliphoridae   Lucilia coeruleiviridis   3,4
Diptera       Muscidae        Hydrotaea leucostoma      4
Diptera       Muscidae        Musca domestica           4

Winter 2009--Coyote

Diptera       Calliphoridae   Phormia regina            3,5,7,9,11,
                                                          15-16,22
Diptera       Calliphoridae   Lucilia coeruleiviridis   3,9,11,34
Diptera       Muscidae        Hydrotaea leucostoma      5,9,16
Hymenoptera   Formicidae      Solenopsis invicta        5
Diptera       Calliphoridae   Calliphora vicina         7
Diptera       Muscidae        Musca domestica           7,37
Diptera       Piophilidae     Piophila casei            7
Diptera       Calliphoridae   Chrysomya rufifacies      7,9,11
Diptera       Calliphoridae   Cynomyopsis cadaverina    9
Diptera       Calliphoridae   Chrysomya megacephala     11
Coleoptera    Staphylinidae   Creophilus maxillosus     15-16,30,34
Coleoptera    Histeridae      Hister spp.               15
Coleoptera    Cleridae        Necrobia rufipes          16
Coleoptera    Histeridae      *                         17
Coleoptera    Dermestidae     *                         17
Diptera       Drosophilidae   Drosophila spp. **        22
Diptera       Muscidae        Fannia cannicularis       22
Coleoptera    Staphylinidae   *                         22
Hymenoptera   Chalcididae     *                         22
Diptera       Sarcophagidae   Sarcophaga spp.           22
Diptera       Muscidae        Fannia scalaris           25
Hymenoptera   Sphecidae       *                         30
Hymenoptera   Vespidae        *                         30
Hymenoptera   Vespidae        Vespula maculifrons       30
Coleoptera    Curculionidae   Diaprepes                 30
                                abbreviates **
Coleoptera    Dermestidae     Dermestes ater            30
Blattodea     Blattidae       Periplaneta               30
                                americana **
Blattodea     Blattidae       Blatta orientalis **      30
Blattodea     Blattidae       *                         30
Diptera       Muscidae        Fannia                    37
Diptera       Psychodidae     *                         44

Spring 2010--Raccoon

Hymenoptera   Formicidae      Solenopsis invicta        1-3,11,14
                                                          -15,17-18
Diptera       Muscidae        Hydrotaea leucostoma      2-4,8
Diptera       Muscidae        Synthesiomyia nudiseta    2-3
Diptera       Calliphoridae   Phormia regina            3-4,7-11
Diptera       Phoridae        Megaselia scalaris        3
Diptera       Calliphoridae   Lucilia coeruleiviridis   4,8
Diptera       Ulidiidae       Chaetopsis spp. **        7,11
Diptera       Muscidae        Musca domestica           7-11,14-15,17
Diptera       Calliphoridae   Chrysomya rufifacies      7-11
Diptera       Tabanidae       Diachlorus                10
                                ferrugatus **
Diptera       Piophilidae     *                         15

Fall 2010--Raccoon

Hymenoptera   Formicidae      Solenopsis invicta        1,3,6,9,13
Diptera       Calliphoridae   Chrysomya rufifacies      6,8-10,13-15
Coleoptera    *               *                         7
Diptera       Muscidae        Musca domestica           9-10,14-15
Diptera       Fanniidae       Fannia spp.               15

Summer 2010--Opossum

Hymenoptera   Formicidae      Solenopsis invicta        1-5
Diptera       Sarcophagidae   Sarcophaga                2
                                hemmorrhoidalis
Diptera       Muscidae        Hydrotaea leucostoma      2-3
Diptera       Calliphoridae   Lucilia coeruleiviridis   2-3
Diptera       Calliphoridae   Cochliomyia macellaria    2
Diptera       Calliphoridae   Phormia regina            2-3
Diptera       Calliphoridae   Chrysomya rufifacies      3-5
Diptera       Ulidiidae       Chaetopsis spp. **        4

* not identified

** not of forensic importance


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Author:Richards, Stephanie L.; Connelly, C. Roxanne; Day, Jonathan F.; Hope, Timothy; Ortiz, Ricardo
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Date:Jun 1, 2015
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