An Analysis of Dung Beetle (Coleoptera: Scarabaeidae: Scarabaeinae & Aphodiinae) Attraction to Small Mammal Carrion

HEADS OR TAILS: AN ANALYSIS OF DUNG BEETLE (COLEOPTERA: SCARABAEIDAE: SCARABAEINAE & APHODIINAE) ATTRACTION TO SMALL MAMMAL CARRION

A Thesis by Rachel Stone Bachelor of Science, Wichita State University, 2013

Submitted to the Department of Biological Sciences and the faculty of the Graduate School of Wichita State University in partial fulfillment of the requirements for the degree of Master of Science

May 2018

HEADS OR TAILS: AN ANALYSIS OF DUNG BEETLE (COLEOPTERA: SCARABAEIDAE: SCARABAEINAE & APHODIINAE) ATTRACTION TO SMALL MAMMAL CARRION

The following faculty members have examined the final copy of this thesis for form and content, and recommend that it be accepted in partial fulfillment of the requirement for the degree of Master of Science with a major in Biological Sciences.

______Mary Jameson, Committee Chair

______Leland Russell, Committee Member

______Peer Moore-Jansen, Committee Member

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DEDICATION

To all who have an appreciation for the industriousness, efficiency, and high moral integrity of the humble dung beetle

“If we and the rest of the backboned animals were to disappear overnight, the rest of the world would get on pretty well. But if they were to disappear, the land's ecosystems would collapse. The soil would lose its fertility. Many of the plants would no longer be pollinated. Lots of animals, amphibians, reptiles, birds, mammals would have nothing to eat. And our fields and pastures would be covered with dung and carrion. These small creatures are within a few inches of our feet, wherever we go on land – but often, they're disregarded. We would do very well to remember them.”—David Attenborough

ACKNOWLEDGEMENTS

This project could not have been possible without the contributions of Emmy Engasser

(with whom I’m honored to share the esteemed title of Carrion Queen), the best co-investigator I could have ever hoped for and a person who exemplifies hard work and determination in everything she sets her mind to, as well as Dr. Mary Liz Jameson, my mentor extraordinaire, who has unwaveringly provided valuable knowledge, support, guidance, friendship, and even chocolates in desperate times. I am deeply inspired by the enthusiasm you both have for the natural world and the spirit of generosity you spread. I am truly privileged to have learned from you both.

I would like to thank Dr. Peer Moore-Jansen for his generous monetary support and access to Skeleton Acres Research Facility. I would also like to thank Dr. Leland Russell for his statistical prowess and willingness to share in his knowledge. Thank you to Ranger Randy Just and Seth

Turner (Kansas Department of Wildlife, Parks and Tourism) for access to El Dorado State Park, and to Joyce Dudeck, Kim and Scott Bays for sharing their beautiful 80-acre plot. Thanks also to

Larry Slayton at the Sedgwick County Zoo for his ability to provide us with a seemingly unending supply of frozen rats. I am so deeply grateful to the many helpful research assistants both in the field and in the lab, who spent their time contributing to this research: Breanna Sayers, Morgan

Trible, Brandon Hein, Niall Horton, Ethan Grennan, Hannah Hoetmer, Jacqueline Nascimento-

Odenheimer, and Jacqueline Baum. I am humbled by your generosity and dedication to this ambitious project and I am so thankful for the friendships this work has fostered. Thanks also to my dear old dad, Brian Stone, a constant source of encouragement and sincere belief in my ability; everybody needs someone in their corner, and I am so glad that you are in mine. It takes a village to tackle such a project, to all the others who have in any way aided in the development and execution of this project: Thank YOU!

ABSTRACT

Necrophilous insects occupy a biologically interesting ecological niche because carrion is a highly desirable but ephemeral food source. Insects that feed on carrion are widely studied in forensic and entomological disciplines, but many taxa attracted to decomposition are often overlooked. Dung beetles (Coleoptera: Scarabaeidae: Scarabaeinae and Aphodiinae) are frequently found at carrion, but very little is known about their attraction to this resource. Are dung beetles attracted to the carrion itself or are they attracted indirectly because the gastrointestinal contents of the animals are exposed? This research attempts to disentangle the association between dung beetles and carrion by examining the distribution of dung beetles on the head- and tail-end of rat carrion, delimiting a resource more attractive to necrophagous insects (head-end) and a resource more attractive to coprophagous insects (tail-end). Comparisons were made between dung beetle distributions on rat carrion with carrion beetle (Coleoptera: Silphidae) distributions, a model of distribution patterns for a taxon known to target carrion. A total of 25,081 dung beetle individuals from 21 species and 3,333 individual carrion beetles from 9 species were collected in our year-long study. Results indicate that dung beetles show higher attraction to the head-end of rat carrion than the tail-end. This distribution pattern is also found in carrion beetles, suggesting that similar resources are being targeted. When dung beetles are grouped by behavioral guilds, rollers and tunnellers also share this pattern of greater abundance at the head-end rather than the tail-end, but dwellers show no discernable difference between the head- and tail-end. This research indicates that dung beetle interactions with carrion that are more complex than previously understood. Our results suggest that scarabaeine dung beetles target carrion preferentially, challenging the long-held belief that, within temperate regions, dung beetle necrophagy is rare and unimportant to the decomposition of carrion.

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TABLE OF CONTENTS

Chapter Page

1. INTRODUCTION…………………………….……………….…………………...... 1

1.1 Introduction……………….………………………….…………………………....1 1.2 Questions and Significance……………..…………………………………….…...7

2. MATERIALS AND METHODS………………………..………………………..……...11

2.1 Study Sites……………………….……….……………………………………....11 2.2 Insect Sampling……………………..…………………………………………....13 2.3 Abiotic Measurements…………….……………………………………….…….15 2.4 Laboratory Methods……...……………………..………………………………..16 2.5 Data Analyses…………..………………………………………………………...17

3. RESULTS…………………………………..…………………………………………....24

3.1 Diversity Results………………………..……………………………..………....24 3.2 Phenology Results…………………………………..………………..…………..26

4. DISCUSSION………..…………………………………………………………….…….34

4.1 Discussion………………………………………..……………………………....34 4.2 Significance…………..……………………………………………………..…....39

REFERENCES…………………………………………………………………………………..42

APPENDICES……………………………………………………………………….…………..52

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LIST OF TABLES

Table Page

1. Research site locations…………………………………………….……………………..19

2. Collection episode by date range and season…………………………………………….23

3. Dung beetle species and their abundances……………………………………………….28

4. Carrion beetle species and their abundances…………………………………………….28

5. Biodiversity metrics for dung beetles and carrion beetles……………………………….29

6. Mixed model ANOVA results…………………………………………………………...31

7. Abiotic factors……………………………………………………………………………33

LIST OF FIGURES

Figure Page

1. Illustration of dung beetle guilds…………………………………...…………...……….10

2. Overview of transect design……………………………………………………………...22

3. Overview of pit fall trap design……………………………………………...…………..22

4. Wire exclosure design……………………………………………………………………23

5. Biodiversity profiles of dung beetle communities………………………...……………..29

6. Biodiversity profiles of carrion beetle communities…………...………………………...29

7. Average dung beetle and carrion beetle abundances………….…………...…………….30

8. Average abundances of dung beetle guilds………………………………………………30

9. Dung beetle phenology………………………………………...………………………...31

10. Carrion beetle phenology………………………………………………………………...32

LIST OF MAPS

Map Page

1. Physiographic map of Kansas……………………...………………………………...…..19

2. El Dorado State Park……………………………………………………………………..20

3. Skeleton Acres Research Facility………………………………...……………………...20

4. The 80 Acres……………………………………………………………………………..21

5. View of all research sites…………………………………...……………………………21

LIST OF PLATES

Plate Page

1. Exemplar Scarabaeidae of Kansas……………………………………………………..….9

2. Dung beetle roller behavior……………………………………………………………...10

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CHAPTER 1

INTRODUCTION

1.1 Introduction

The vast majority of Scarabaeidae are either phytophagous or coprophagous, but many scarab beetles, particularly in the dung-feeding guild (Scarabaeinae and Aphodiinae: Scarabaeidae:

Coleoptera) (Plate 1), are regularly represented in carrion-baited traps (Braack 1986; Ratcliffe and

Paulsen 2008; Villet 2011; Whipple et al. 2012; Ratcliffe 2013). Researchers have previously hypothesized that their attraction is not to carrion itself, but to the contents within the gastrointestinal tract that become exposed during carcass decomposition (Midgley et al. 2012).

However, the mechanisms of scarab attraction to carrion are not well understood. In fact, even the components of excrement that adult dung beetles utilize for food is poorly understood, except that it is sourced from fresh dung. The inspection of adult dung beetle gut contents reveals a liquid but viscous suspension of microscopic particles (Madle 1934; Miller 1961). More recent evidence indicates these fine particles are primarily bacteria and dead epithelial cells from the herbivore’s gut, indicating that tiny particles are preferentially selected while larger components of dung substrate such as coarse plant fibers are rejected by adult dung beetles (Holter and Scholtz 2007).

However, the fibrous component of dung is utilized by dung beetle larvae and is an important material for larval brooding (Halffter and Matthews 1966; Halffter and Edmonds 1982).

Although, coprophagy is well known among dung beetles, necrophagy has been documented on both vertebrate and invertebrate carrion in tropical regions of South America and

Africa (Cornaby 1974; Braack 1986; Favila and Díaz 1996; Amézquita and Favila 2011; Villet

2011; Cantil et al. 2014; González-Vainer 2015). Within these regions, large herbivores and the dung they produce are lacking. Past studies have demonstrated that herbivore biomass is highest

1 in grasslands in comparison to tropical habitats (Odum et al. 1970; Fittkau and Klinge 1973;

Montgomery and Sunquist 1975) and temperate forest habitats (Turček 1969). Ostensibly, dung beetle necrophagy was necessarily adopted due to the paucity of herbivore dung in the tropics.

Further, the necrophagous beetle group, Silphidae, does not have a distribution that extends to the equator (Ratcliffe 1996). Consequently, the lack of a necrophagous invertebrate counterpart in the tropics creates a vacant niche for dung beetles to fill. This, however, does not explain why dung beetles are frequently associated with carrion-baited traps in temperate regions far beyond the equator where Silphidae, or carrion beetles, occur (Ratcliffe 1996; Benbow et al. 2016). This regular occurrence is often disregarded, in fact instances of carrion-feeding by dung beetles outside of the tropics have been deemed “occasional and unimportant” (Halffter and Matthews 1966). In this study, we challenge this long-held notion by investigating dung beetle attraction to rat carrion in a region well within the range of carrion beetle distribution (Lingafelter 1995), and where large herbivores, in the form of domestic cattle, abound. Grazing cattle pastures, which were adjacent to all study sites, are known for the stable dung availability they provide (about 12 pats per animal per day [Hancock 1953]).

Both the deposition of dung and the death of an animal initiate an intricate ecological web of interactions between decomposers, scavengers, opportunistic predators, and parasitoids

(Putman 1983; Benbow et al. 2016). Of these trophic groups, decomposers are one of the most important contributors in any ecological system, salvaging the raw materials and resources that are tied up in waste and rendering them biologically available to the community. In terms of the total energetic contribution to a community, decomposers fill the most substantial role of any trophic assemblage, being responsible for more than 95% of overall community metabolism in most terrestrial systems (Putman 1983). Leaf litter systems are given more attention in the literature than

2 carrion and dung (Melillo et al. 1982; Aerts 1997; Gartner and Cardon 2004; Hättenschwiler et al.

2005; Cornelissen et al. 2007). Litter systems receive considerably more investigation of decay processes, the influence of abiotic factors on the rate of decomposition, and the myriad different roles of organisms which contribute to decay, while carrion and dung systems, for rather glaringly obvious reasons, are eschewed and still require detailed investigation to establish and fully describe the highly specialized communities associated with such ephemeral resources.

Dung and carrion represent highly specialized ecological units, defined and bounded, supporting an entirely distinctive assemblage of organisms and forming their own characteristic communities (Putman 1983; Hanski and Cambefort 1991; Benbow et al. 2016). Many properties are shared between dung and carrion and distinguish these food sources from others. In fact, a number of invertebrate species, primarily generalist true flies (Diptera), are known to utilize both dung and carrion interchangeably as a resource (Byrd and Castner 2010). Dung and carrion are highly ephemeral and unpredictable in nature, creating patchily-distributed “islands” of high- quality resources within an ecosystem (Stephens and Krebs 1986; Hanski and Cambefort 1991).

Dung and carrion are also nutritionally rich with high concentrations of micronutrients like nitrogen and carbon (Swift et al. 1979; Moore et al. 2004; Yamada et al. 2007), bacteria, and fungi

(Holter and Scholtz 2007). Carrion is a particularly protein-rich food source (Benbow et al. 2016), while herbivore dung is rich in vitamins (McBee 1971), minerals (Olechowicz 1974), and products of the gut fauna and flora (Lambourne and Reardon 1962; Anderson and Coe 1974). Owing to these qualities, dung and carrion are highly coveted nutrient resources and are often the source of intense competition among those that utilize it (Hanksi and Cambefort 1991; Benbow et al. 2016).

This severe competition is the main force structuring these ephemeral communities (Hanski 1987).

The resource islands that comprise ephemeral habitats are fiercely contested. In response, dung beetles have developed various behavioral tactics to gain access to their share of the resource.

The three mostly commonly defined dung beetle guilds can be distinguished as: the tunnellers, the dwellers, and the rollers (Figure 1; Floate 2011). While these groupings are not necessarily evolutionarily informative, they are behaviorally and functionally meaningful in their classification (Halffter and Edmonds 1982; Ratcliffe and Paulsen 2008). Most tribes of

Scarabaeinae in the United States are tunnellers: they excavate burrows immediately below the dung pat, which they then provision with the dung from above to be used for either adult feeding or for breeding (Hanski and Cambefort 1991). The dwellers are endocoprophagous, meaning they live and feed within the dung pat itself. Aphodiinae, a subfamily comprised of typically small, temperate dung beetles, represent the bulk of the dwellers: they tunnel directly into dung, and deposit their eggs in the dung pats without any kind of relocation behavior (Ratcliffe and Paulsen

2008). Finally, some tribes within Scarabaeinae have evolved the remarkable skill of forming a ball of dung from a larger heap, using their head and forelegs as a shovel, then rolling the ball away from the dung pat and competing beetles, before concealing underground for use as either a brood ball or an adult food ball (Plate 2). This behavior quickly removes the dung from the area of intense competition and lowers the risk of brood parasitism and kleptoparasitism (González-

Megías and Sánchez-Piñero 2003; 2004).

Dung beetles are observed to be highly effective in locating patchy food sources, frequently arriving at dung within 1 minute of it being made available (Peck et al. 1984) or employing a sit- and-wait technique at the anus of an animal before dung deposition has even occurred (Jacobs et al. 2008). In one study, researchers observed approximately 4,000 dung beetles arriving at a half- liter dung sample within 15 minutes of exposure (Heinrich and Bartholomew 1979). Numerous

4 investigations indicate that chemoreception is the primary means of dung beetle food perception, with the antennae being the primary organs of chemoreception, and the maxillary palpi being the secondary organs, only used when in contact with the food source (Comignan 1928; Warnke 1934;

Prasse 1957). There is no evidence of visual perception of the food (Heymons and von Lengerken

1929). Adult dung beetles may execute cruising search flights in some cases, but many passively wait with their antennae outstretched until odor cues are detected (Ohaus 1909; Halffter and

Matthews 1966). Once these odor currents are perceived, the beetle will take to flight, moving upwind into the odor current and typically approaching in a direct straight-line flight until it is nearing the source (presumably perceived as a sudden increase in olfactory stimuli intensity)

(Halffter and Matthews 1966). Once at a close range (3-80 cm), many dung beetles will land abruptly and walk the rest of the distance in a straight line, while others will approach the food source flying very low, 30 to 60 cm above the ground surface, in a zig-zag or figure-8 flight pattern along a horizontal plane (Prasse 1957; Halffter and Matthews 1966; Halffter and Edmonds 1982).

Such scarabs display impressively adept, small-scale targeting skills and have been observed landing directly on dung soon after its deposition (Personal Observation of Onthophagus spp. by

Stone 2017). For example, members of the genus Phanaeus have been documented to display remarkably skillful flight behaviors, circling over their food source, approaching to a hover, and landing directly on top (Halffter and Matthews 1966; Edmonds 1994).

The animals that capitalize on patchy resources such as carrion and dung are able to do so, in large part, due to odor cues given off by the food source in the form of volatile organic compounds (Dormont et al. 2010). Numerous studies have found that dung beetles are able to discriminate among various volatile organic compounds (Fincher et al. 1970; Davis 1994;

Dormont et al. 2004). While many volatiles given off by carrion (Statheropoulos et al. 2005), cow

5 dung (Kite 1995), and pig dung (Schaeffer 1977; Yasuhara et al. 1984), for example, are unique and distinguish the sources from each other, some compounds do overlap, primarily skatole and indole (Flechtmann et al. 2009). Since dung beetles do not appear to respond to isolated volatiles but rather to the blend of volatiles associated with a food source (Inouchi et al. 1988), it is thought that dung beetles are able to differentiate between the volatile bouquets released from herbivore dung and those produced by decomposing carrion. Many environmental factors can influence an animal’s ability to detect volatile compounds such as wind speed, air and soil temperature, and soil humidity (Ridsdill-Smith 1991). These environmental factors vary greatly both spatially and temporally. Understanding their impacts on dung beetle community assemblage in response is ecologically important in understanding the structuring of ecological communities (Nichols et al.

2008), nutrient cycling (Hanski 1987), linkages between trophic levels (Simmons and Ridsdill-

Smith 2011), and even community disease control (Fialho et al. 2018). Describing the various dung beetle species visiting carrion over different seasons and habitats can lead to better understanding their responses to such environmental conditions. These abiotic factors likely play a role in foraging and resource detection by dung beetles and have value not only to community ecologists but to a wide range of disciplines from forensic entomology to agronomy.

The placement of an intact, mammal carcass on the ground is, from one perspective, the tidy, parceled offering of two ephemeral resources: carrion is obviously present by definition, as is the dung within the gastrointestinal tract set in the caudal half of the carcass. Necrophagous insects are well known in successional studies to target fresh wounds and any natural orifices found on carrion (Anderson and VanLaerhoven 1996; Anderson and Hobischak 2004; Perez et al. 2005;

Martinez et al. 2007). The majority of natural orifices found on mammal carrion occur frontally, on the head region of the animal, and include the mouth and the paired eyes, external nares, and

6 the ear canal, compared to the occurrence of relatively small natural orifices on the caudal, or tail- end, region: the urogenital orifice and the anus (Daniel 1910). Because most natural orifices of the mammalian body are localized at the head-end, it is likely carrion-feeding invertebrates will preferentially target this region, while those seeking dung will target the tail-end region of a carcass. This study aims to examine dung beetle preference for decomposing flesh or gastrointestinal products associated with rat carcasses by examining assemblages of beetles caught at the head region compared to the tail region of rat carrion. Because scarab beetles are able to target small-scale resources with relatively high accuracy, comparing scarab abundance on head- and tail-ends of rat carcasses can shed light on the object of the insect’s desire: dung or decomposing flesh. Understanding the resources that dung beetles target on carrion will reveal details of scarab biology that are under-researched as well as opening the door for many more studies to explore the relationship between dung beetles and decomposition.

1.2 Questions and Significance

1. Is dung beetle abundance different at the head- and tail-end of rat carrion? A higher

representation of dung beetles at one end of a rat rather than an even distribution would

suggest a specific resource is being targeted. Analyzing head or tail preference at rat

carcasses allows us to discern if dung beetles actively target vertebrate dung only or also

target decomposing tissue. The head is highly targeted by carrion feeders (Perez et al. 2005;

Matuszewski 2010), so those targeting carrion will have a higher representation at the head-

end of a rat carcass. Those targeting dung, which is strongly associated with caudal half of

mammals due to the location of the gastrointestinal tract, will have a higher representation

at the tail-end of a rat carcass.

2. How do dung beetle assemblage patterns at the head- and tail-end of rat carrion

compare to carrion beetle (Silphidae: Coleoptera) assemblage patterns? Carrion

beetles, an unrelated taxonomic group of beetles, are well known to feed on decaying flesh

(Ratcliffe 1996). Because carrion beetles are a necrophagous group, they can serve as a

model of beetle assemblage patterns for a taxon that is known to target carrion as a

resource. If distribution patterns on rat carcasses are similar in dung beetles and carrion

beetles, then this would indicate similar resources are being targeted.

3. Does dung beetle distribution at the head and tail differ by behavioral guilds? The

intense competition that occurs at ephemeral habitats promotes the evolutionary pressure

to partition resources so that multiple species may coexist (Schoener 1974). Dung is a

highly prized resource for those that can capitalize on it, and this has resulted in the

separation of dung beetles into behavioral guilds. By considering head- and tail-end

preference by guild, we can investigate whether resource partitioning pressures have led

guilds to diverge not just behaviorally, but also in the food resources that they target.

4. Do dung beetle and carrion beetle communities at the head- and tail-end of rat carrion

differ in terms of diversity? Abundance, while valuable, does not provide a full picture

of a community. Obtaining detailed biodiversity metrics (such as richness, evenness,

Shannon-Wiener diversity index, and effective species numbers) will help home in on any

differences within the communities that abundance values cannot reveal.

5. Do dung beetles and carrion beetles exhibit differences in seasonal activity? In

temperate regions, most carrion field research takes place only during the warmest times

of the year, having great potential to introduce a foundational bias in our understanding of

invertebrate communities on carrion (Anderson 2010; Benbow et al. 2016). In addition to

answering the above questions, conducting field research for a full calendar year allows us

to investigate the seasonal activity exhibited by scarabs and silphids on carrion in the

Kansas Flint Hills. Phenologies for both taxa are not well-documented for the region and

will provide beneficial information for future studies. While the lack of replication in

seasonal data does not allow us to make clear predictions about future seasonal trends of

these taxa, it does allow us to paint a picture of seasonality for the year in which this study

occurred.

PLATE 1. Exemplar Scarabaeidae of Kansas. Images of typical dung beetles found in Kansas. From left to right: Copris minutus (Drury), Phanaeus vindex MacLeay, Onthophagus knausi Brown, and Copris fricator (Fabricius). Photos by R.L. Stone.

FIGURE 1. Illustration of dung beetle guilds. From Floate (2011).

PLATE 2. Dung beetle roller behavior. Canthon pilularius (Linnaeus) rolling a cattle dung ball away from the dung pat. Photo by R.L. Stone.

CHAPTER 2

MATERIALS AND METHODS

2.1 Study Sites

Two-thirds of the Greater Flint Hills region remains almost entirely natural tallgrass prairie owing to its rocky, uneasily plowed soils (Obermeyer 2014). While this land is rarely plowed for crops, the Flint Hills do serve as an important landscape for supporting grazing cattle year-round

(Anderson and Fly 1955). The presence of year-round, freely available herbivore dung in the region provides a desirable backdrop for the study of dung beetle communities. The Kansas Flint

Hills Uplands physiographic region (Map 1) spans a north-south strip through east-central Kansas and experiences fire and drought as its primary disturbance regimes (Kansas Geological Survey

1999). Although the Flint Hills region is known for its rolling prairie, it is named for the ubiquitous flint embedded in the limestone hills. As the limestone erodes, it breaks down into soil, exposing the flint that is broken down into cherty gravel (Anderson and Fly 1955). Butler County and

Cowley County are found within the Flint Hills ecoregion, nested in south-central Kansas. The average annual temperature for this region is 15°C (Kansas Geological Survey 1999). Annual precipitation is variable with ranges typically between 71-89 cm (28-35 inches) (USFWS 2014).

To account for natural variation across the Flint Hills, three sample sites were selected from two counties within the ecoregion (Table 2): El Dorado State Park within Butler County (37.846°N,

96.827°W)(Map 2), Skeleton Acres Research Facility within Butler County (37.737°N,

96.662°W)(Map 3), and an 80-acre privately owned property near Atlanta, Kansas within Cowley

County (“The 80”; 37.384°N, 96.733°W)(Map 4). Beyond the criteria of being situated within the

Flint Hills ecoregion, the sites were selected based on the presence of both grassland and woodland habitats large enough to accommodate an 80m north-south transect. Woodland and grassland

11 habitats were used in order to account for the inherent variation within the individual sites.

Woodland habitat types were defined as an area with nearly constant canopy cover throughout growing season, and grassland habitat types were defined as an area with no canopy cover and high density of grasses and forbs.

El Dorado State Park (EDSP) is a state park managed by the Kansas Department of

Wildlife, Parks, and Tourism (KDWPT). The park is situated in El Dorado, KS and is comprised of approximately 4500 acres of park lands and 3500 acres of wildlife area with an elevation of

395-402 m (Kansas Department of Wildlife, Parks and Tourism 2018). The property is a popular fishing and boating destination, containing the seventh largest reservoir in Kansas, and is bounded by wildlife areas composed of grasslands and woodlands. The area surrounding the state park consists of urban development, privately owned residences, and grazing pastures. Following acquisition of the property in 1981, KDWPT seeded grasslands with native plant species. The land management regime consists of a combination of haying, mowing, and patch burning every 2-3 years. The last controlled burn prior to our study occurred in 2014 (Seth Turner, February 2017,

Personal Communication).

Skeleton Acres Research Facility (SARF) is the smallest of the study sites at 7.5 acres. The property is located near Leon, KS and is at an elevation of approximately 430-445 m. Previously a privately-owned plot, SARF was acquired as a permanent easement for the Anthropology

Department of Wichita State University in 2004. It is now used primarily for forensic anthropology research purposes. The property occasionally is used for decomposition research and has been subjected to some small carrion deposition in localized areas prior to this study. Within the site, a small plot was tilled until 2011 for planting of wheat and corn. The area surrounding the research facility consists of agricultural plots, privately owned residences, and grazing pastures. The land

12 management regime consists of mowing twice a year, once in March-April and once in September-

October. Controlled burning is not practiced at this site, but in recent history accidental burns occurred in mid-April of 2016 and 2017 (Peer Moore-Jansen, February 2017, Personal

Communication).

“The 80”, as its name suggests, is an 80-acre privately-owned property located in Atlanta,

KS. The property is at an elevation of 427-439 m and contains woodland prairie habitat and an intermittent creek. The areas surrounding the property are used for pastures and grazing. The 80 was acquired by its current owners in 1993. The land management regime consists of haying annually in the summer season. Controlled burning is not practiced at this site, and no record of accidental burns is known. The site has an agricultural history; milo, corn, and soybeans have been grown near the placement of our transects but were not present at the time of the study (Scott and

Kim Bays, January 2017, Personal Communication).

2.2 Insect Sampling

Each north-south transect was 80 m in length with eight points every 10 m (Figure 2). Of these points, the two end points were unbaited controls, and the remaining six points were baited with a single rat (Rattus norvegicus) carcass. The head of each carcass was oriented toward the west and the tail pointing east. Two pitfall traps occurred at each point, one west (the head-end of a baited point) and one east (the tail-end of a baited point). With three sites, each with two transects, this sampling design resulted in a total of 48 points and 96 samples for each monthly deployment for an entire year. Large (174g to 274g) rat carcasses were provided from MiceDirect (Cleveland,

GA, www.micedirect.com). Each rat was 43-60 days old, was fed a Mazuri® diet, and was euthanized by CO2 gas. Rats were stored at 0°C to -20°C. Twenty-four hours before deployment,

13 rats were thawed at room temperature. Rat carcasses were placed laterally between the pitfall traps to expose portions of both the ventral and dorsal surfaces.

Pitfall trap design (Figure 3) consisted of two 946ml (32 fluid ounces) plastic cups: an outer cup with holes drilled on the bottom and sides along with an inner cup with two holes only on the sides. When the inner cup is placed inside the outer, the holes along the side are aligned; this allowed rainwater to drain into the ground rather than overflow the trap. Pitfall traps were placed in dug holes flush with the surface of the ground. The cups were filled with approximately 160 ml of a 50-50 mixture of propylene glycol (99.9% USP grade) and tap water. Pitfall traps were covered by a plastic lid with a quarter wedge cut out, creating a triangular opening that was positioned toward the rat carcass. The lid design reduced rainwater entry and helped to direct insects into the preservative mixture within the pitfall trap. The points along the transect were completely covered with a hardware cloth exclosure (Figure 4) with a 1cm mesh to discourage scavenging by vertebrates while allowing insects to pass through easily. Exclosures were held together with UV resistant zip ties and kept anchored to the ground surface with garden staples.

Collection period refers to the time between fresh carcass deployment and retrieval. Each collection period occurred over the course of four weeks for a total of 12 months, allowing for collection of the full succession of carrion-attracted insects through all decomposition stages of rat carrion. Studies have found that complete decomposition of rat carrion takes up to 22 days in a temperate zone (Kočárek 2003, Tomberlin and Adler 1998). Every four weeks a new rat carcass was deployed, abiotic habitat variables were recorded, and pitfall traps were collected and replaced. Any remains from the previously decayed rat carcass were removed from the site to avoid sampling bias. Over the course of the study, 13 serial collection episodes took place (Table

2), with fresh rat carrion and pit fall traps deployed at the start, and carcass removal and pit fall

14 traps retrieved at the end of the period (May 28, 2016 – May 29, 2017). Each collection period spanned 28 full days, with the exception of the final collection episode in which all three sites were visited on separate days in order to accommodate the time constraints of an auxiliary study set to begin immediately following removal of the final carcass at every point. This slight adjustment resulted in the final collection episode encompassing 28 days for EDSP (retrieval on May 27,

2017), 29 days for the 80-acre (retrieval on May 28, 2017), and 30 days for SARF (retrieval on

May 29, 2017).

2.3 Abiotic Measurements

Four abiotic habitat variables were selected due to their potential to influence decomposition rates and insect detection: light penetration, wind speed, soil surface humidity, and soil surface temperature. These variables were recorded at every point along the transect every time a fresh rat carcass was deployed (Table 2). To measure light penetration that reaches each carcass, a light ceptometer (Decagon Devices, Inc. AccuPAR PAR/LAI model LP-80, Pullman,

WA, www.decagon.com) was used to measure photosynthetically active radiation (PAR). PAR was recorded from the top of the exclosure at each point to ensure light receptors were kept at a uniform distance from ground (15 cm from the surface of the ground). Three separate readings were taken at 30 second intervals so that an average PAR value could be calculated for each point.

Light ceptometer readings were recorded between 9:30 to 15:00. To measure wind speed at each point, an anemometer (Nielsen-Kellerman Kestrel 1000, Boothwyn, PA, www.NKhome.com) was used. The device was held 0.91 meters (the length of a yardstick) above each point, facing the direction of the prevailing wind. Wind speed was measured for a total of one minute, and both average and maximum wind speeds (in meters/sec) were recorded. Soil surface humidity and soil surface temperature were recorded at each point using an external thermometer-hygrometer (H-B

Instruments DURAC 3735 Hygro-Thermometer, Wayne, NJ, www.belart.com). The external probe was placed on the top of the soil near the sternum of the rat carcass and allowed to equilibrate for 5 minutes; humidity and temperature were then recorded.

2.4 Laboratory Methods

Contents of pitfall traps were brought into the laboratory and sorted using a dissecting microscope (Leica M80 0.8x-1.0x Achromatic lens, Buffalo Grove, IL, http://www.leica- microsystems.com). Targeted insect taxa, the carrion-attracted beetle families (Coleoptera:

Silphidae, Staphylinidae, Trogidae, Histeridae, Dermestidae, and Scarabaeidae), and by-catch

(non-target insects) were separated for further examination. Once separated, species-level identifications were made for all adult silphid specimens using available identification keys

(Anderson and Peck 1985, Ratcliffe 1996, Monk et al. 2016, Smith 2016). Adult scarab specimens from the subfamilies Scarabaeinae and Aphodiinae (dung beetles) were also identified to species level using identification keys (Ratcliffe and Paulsen 2008, Arnett et al. 2002) as well as the

Wichita State University Invertebrate Collection (WICHI) and the Division of Entomology at the

University of Nebraska State Museum (UNSM) for comparative identification. Genera were then categorized by behavioral guild (Halffter and Matthews 1966, Halffter and Edmonds 1982, Hanski and Cambefort 1991). Abundance and species richness were recorded and organized in Microsoft

Excel (version 15.20). Voucher specimens are deposited at the following invertebrate collections:

Wichita State University Invertebrate Collection (WICHI), Division of Entomology at the

University of Nebraska State in Lincoln (UNSM), Snow Entomological Museum Collection at

University of Kansas (SEMC), and the Kansas State University Museum of Entomological and

Prairie Arthropod Research (KSU-MEPAR).

2.5 Data Analyses

For every pitfall trap sample, the date of collection, site, habitat, and head/tail orientation were recorded. The date of collection was used in organizing phenology data, and seasons were determined by solstice (summer and winter) and equinox (spring and fall) events (National

Weather Service 2018). From each sample, the species richness (number of species) and abundance (number of individuals per species) were recorded. These data were used to examine relationships between pitfall trap orientation and beetle community structure among taxa.

Assigning individual rat carcasses as a random effect, a mixed model ANOVA (“lme4” [Bates et al. 2015] and “lmerTest” [Kuznetsova et al. 2016] in RStudio [R Core Team 2015]) was used to investigate the significance of differences between scarab and silphid abundances at the head- and tail-positioned pit fall traps. R (version 3.3.2) was used to calculate the evenness (J) and Shannon-

Weiner (H) species diversity index for head and tail orientations (“vegan” in RStudio [Oksanen et al. 2016]). Shannon-Weiner values are widely used to characterize biological diversity and provide an index of species diversity that considers species richness and the distribution of abundance of species in its model (Spellerberg and Fedor 2003). Biodiversity indices provide some context but do not necessarily give clear, easy-to-interpret results because they are unitless, nonlinear values

(Jost 2006). To facilitate interpretation of results, Shannon-Weiner values (H) were transformed to effective species numbers (exp(H)), a technique that provides a measure of true diversity by weighing values by their frequency without disproportionately favoring rare or common elements

(Jost 2006). As such, effective species numbers convey true diversity of a community by providing the number of species with identical frequencies that would give the same level of diversity as the data. Diversity profiles were built in R to provide a visual characterization of the relative contributions of evenness and richness to scarabs and silphids attracted to rat carrion. Diversity

17 profiles provide a comprehensive presentation of all biodiversity information about a community and are fundamental in the analysis of diversity as well as making comparisons between communities (Chao et al. 2014).

MAP 1: Physiographic Map of Kansas. Note the region of interest, the Flint Hills Uplands, indicated in yellow (Kansas Geological Survey 1997).

TABLE 1. Research site locations.

Site Location El Dorado State Park El Dorado, Butler County, KS

(EDSP) (37.846°N, 96.827°W)

Skeleton Acres Research Facility (SARF) Leon, Butler County, KS

(37.737°N, 96.662°W)

The 80 Acres (80) Atlanta, Cowley County, KS

(37.384°N, 96.733°W)

MAP 2. El Dorado State Park. Site with transects indicated with white lines. Satellite image from Google Earth 2017.

MAP 3. Skeleton Acres Research Facility. Site with transects indicated with white lines. Satellite image from Google Earth 2017.

MAP 4. The 80 Acres. Site with transects indicated with white lines. Satellite image from Google Earth 2017.

MAP 5. View of all research sites. Satellite image from Google Earth 2017.

FIGURE 2. Overview of transect design. Each 80 m transect contained 8 points separated by 10 m; 6 points were baited with rat carrion and 2 control points on either end without rat carrion. At every point, two pitfall traps were placed near the frontal and caudal end of the rat. Image created by E.L. Engasser.

FIGURE 3. Overview of pit fall trap design. Drilled holes indicated in red. Cup on left (inner cup) is inserted into cup on right (outer cup), and the holes on the sides are aligned. The placement of drilled holes prevents overflow of rainwater that could otherwise lead to losing insects specimens trapped within. Image created by R.L. Stone.

FIGURE 4. Wire exclosure design. Cuts indicated with red lines and bends with black (dimensions in inches). Exclosure materials included 1 cm mesh hardware cloth and UV-resistant zip ties to hold its shape. These were placed over every point along a transect and secured with garden staples with the intention of preventing vertebrate thievery of rat carrion. Image created by R.L. Stone.

TABLE 2. Collection episode by date range and season. The first date of the range indicates deployment of a fresh rat carcass and pitfall traps, and the end of the range indicates the date of removal of carrion remains and pitfall trap retrieval. Seasons were determined by solstice (summer and winter) and equinox (spring and fall) events (National Weather Service 2018).

Collection Episode Approximate Season Collection Period (Deployment-Retrieval) 1 Spring May 28-June 25, 2016 Episode 2 Summer June 25-July 23, 2016 3 July 23-August 20, 2016 4 August 20-September 17, 2016 5 Fall September 17-October 15, 2016 6 October 15-November 12, 2016 7 November 12-December 10, 2016 8 Winter December 10, 2016-January 7, 2017 9 January 7- February 4, 2017 10 February 4-March 4, 2017 11 Spring March 4-April 1, 2017 12 April 1- May 2, 2017 13 May 2-May 27, 28, & 29, 2017

CHAPTER 3

RESULTS

3.1 Diversity Results

Our year-long series of collection periods resulted in 25,081 scarabaeine and aphodiine

(Scarabaeinae and Aphodiinae: Scarabaeidae: Coleoptera) individuals from 21 total species (Table

3) and 3,333 individual silphids (Silphidae: Coleoptera) from 9 species (Table 4). Of the 21 total scarab species, 8 species belonged to the tunneller guild, 3 species to the roller guild, and 10 species to the dweller guild (Table 3). Abundance, richness, evenness, Shannon-Wiener diversity indices, and effective species numbers were calculated to characterize scarab and silphid communities at the frontal (=oriented at the head-end) and caudal (=oriented at the tail-end) traps (Table 4). The abundances for both scarabs and silphids were higher at the head-end than at the tail-end of rat carrion. Richness at the head and tail was equal for silphids (9 species found in both positions) and nearly equal for scarabs with 20 species found in head-oriented traps and 21 in tail-oriented traps.

The scarab community was moderately even at the head and tail (J=0.579 and 0.588, respectively).

The silphid community was more even than scarabs; evenness was most strong in the silphid community at the tail-end (J=0.725) in contrast with the head-end (J=0.659). Shannon-Wiener diversity indices and effective species numbers revealed similar trends for the scarab and silphid communities. Diversities are slightly higher at the tail than at the head region for both taxa. The scarab tail community was the most diverse group (H=1.791, exp(H)=5.996) and the silphid head community was the least diverse (H=1.448, exp(H)=4.256).

Diversity profiles were generated in R to characterize diversity at the head- and tail-end of rat carrion for scarab communities (Figure 5) and silphid communities (Figure 6). Diversity profiles plot effective species numbers on a single graph as a continuous function of the parameter

24 q. Small orders of q give more weight to rare species. For example, when q=0, the diversity equals richness. Large orders of q give more weight to dominant species, for example when q=3, the diversity equals Simpson’s diversity. The overall steepness of the slope illustrates the degree of dominance found within the community; a very steep slope can be interpreted as a highly uneven community, and a horizontal slope indicates a completely even community. Our data show head compared to tail communities are similar in terms of diversity for both scarabs and silphids, but the scarab and silphid communities are distinct from each other. The scarab community, regardless of head or tail position, is more rich, diverse, and uneven than the silphid community (Figures 5-

6).

Abundance data for scarabs and silphids at all sites and habitats were pooled to investigate average abundances at the head and tail of an individual rat carcass set within a single transect point (Figure 2). Mean abundance for both scarabs and silphids is higher at the head than at the tail of rat carrion. The average head-positioned trap had 35.97 individual scarabs and 4.70 individual silphids, and the average tail-positioned trap had 25.77 individual scarabs and 3.14 individual silphids. A mixed model ANOVA found that the effect of head and tail position on scarab abundance is significant (P=0.002), and the effect of head and tail position on silphid abundance is highly significant (P=0.00002) (Table 6). Interactions between head and tail orientation and scarab abundance were further examined by dividing this highly diverse taxon into its behavioral guilds (Appendix Table B). Head and tail position was found to have an effect on tunneller and roller abundances (P=0.02 and 0.01, respectively), but no interaction was detected for the dweller guild (P=0.55). In order to verify the presence of carrion attracted dung beetles to the pit fall traps, the interaction of head and tail traps and abundance at unbaited control points was also investigated; no effect was found (P=0.21).

3.2 Phenology Results

The phenology of scarabs (Figure 9) and silphids (Figure 10) collected for the duration of our year-long study (May 28, 2016 – May 29, 2017) was investigated by recording abundances for every collection period (Table 2). Scarabs of all three guilds were most abundant in the summer collection months with the highest number, 8,550 individuals, caught in the third collection period

(July 23 – August 20, 2016). Scarabs were found every month throughout the year (Appendix

Table A), but abundances decreased drastically in the winter season through early spring with as few as two individuals caught during the ninth collection period (January 7 – February 4, 2017).

Silphids were most abundant earlier in the season than scarabs with the highest number of individuals collected during the first collection period (May 28 – June 25, 2016). Only two individual silphids were collected in the seventh collection period (November 12 – December 10,

2016) and none was found in the eighth and nineth collection periods (December 10, 2016 –

January 7, 2017 and January 7 – February 4, 2017). While scarabs remained active throughout the winter, silphids appeared in higher numbers earlier in the year than scarabs, with 506 silphids compared to only 5 scarabs collected in the tenth collection period (February 4 – March 4, 2017) and 596 silphids compared to 25 scarabs during the eleventh collection period (March 4 – April 1,

2017).

Abiotic factors documented at every collection period (Table 7) revealed a range of temperatures -4.40 °C to 49.30 °C throughout the year and an average of 18.56 °C for the duration of the study. Investigation of abiotic variables grouped by season revealed a summer period (data collected from June 25 – September 17, 2016) with the warmest average soil surface temperature at 29.92°C as well as the highest average light penetration of photosynthetically active radiation

(PAR) at 738.49 µmol m-2 s-1. The fall season (data collected from October 15 – December 10,

2016) was characterized by the highest average soil surface humidity at 67.70% and the lowest average windspeed at 1.03 m/s. The winter season (data collected from January 7 – March 4, 2017) experienced the coldest and least humid soil surface conditions with the average temperature at

3.49°C and average humidity at 39.44%. The winter season also was characterized by the lowest documented PAR values with an average of 367.19 µmol m-2 s-1. The spring season (data collected from April 1 – May 29, 2017) experienced moderate soil surface temperatures and humidity levels

(averages of 15.89°C and 54.34%, respectively), but the highest windspeeds (average of 3.26 m/s) as is typical of the central Kansas region (Kansas Agricultural Experiment Station, 1942).

TABLE 3. Dung beetle species and their abundances. All specimens were collected at carrion- baited traps.

Subfamily Species Total Guild Scarabaeinae Ateuchus histeroides Weber 671 Tunneller

Copris minutus (Drury) 1,158

Copris fricator (Fabricius) 122

Onthophagus hecate (Panzer) 5,125

Onthophagus knausi Brown 1,088

Onthophagus orpheus pseudorpheus Howden & Cartwright 123

Onthophagus pennysylvanicus Harold 11,021

Phanaeus vindex MacLeay 69

Canthon pilularius (Linnaeus) 2,312 Roller

Canthon viridis (Palisot de Beauvois) 297

Pseudocanthon perplexus (LeConte) 771

Aphodiinae Aphodius bicolor Say 158 Dweller

Aphodius erraticus (Linnaeus) 2

Aphodius femoralis Say 3

Aphodius lividus (Olivier) 2

Aphodius pseudolividus Balthasar 9

Aphodius rusicola Melsheimer 2

Aphodius terminalis Say 5

Ataenius spretulus (Haldeman) 2

Ataenius strigatus (Say) 26

Pseudataenius socialis (Horn) 2,115

21 total species 25,081

TABLE 4. Carrion beetle species and their abundances. All specimens were collected at carrion- baited traps.

Subfamily Species Total Silphinae Necrodes surinamensis (Fabricius) 105

Necrophila americana (Linnaeus) 240

Oiceoptoma inequale (Fabricius) 1,795

Oiceoptoma novaboracense (Forster) 143

Thanatophilus truncatus (Say) 2

Nicrophorinae Nicrophorus marginatus Fabricius 208

Nicrophorus orbicollis Say 488

Nicrophorus pustulatus Herschel 55

Nicrophorus tomentosus Weber 297

9 total species 3,333

TABLE 5. Biodiversity metrics for dung beetles and carrion beetles. Data organized by the head- and tail-end.

Scarabs Silphids Head Tail Head Tail Abundance 14,614 10,467 2,026 1,307 Richness 20 21 9 9 Pielou’s Evenness (J) 0.579 0.588 0.659 0.725 S-W Diversity Index (H) 1.733 1.791 1.448 1.594 Effective Species Number 5.659 5.996 4.256 4.922

FIGURE 5. Biodiversity profiles of dung beetle communities. Data organized by head-end and tail-end of rat carrion.

FIGURE 6. Biodiversity profiles of carrion beetle communities. Data organized by head- and tail- end of rat carrion.

FIGURE 7. Average (± Standard error) dung beetle (scarab) and carrion beetle (silphid) abundances. Data organized by head- and tail-end of rat carrion

FIGURE 8. Average (± Standard error) abundances of dung beetle guilds. Data organized by head- and tail-end of rat carrion

TABLE 6. Mixed model ANOVA results. Investigating head and tail trap orientation effect on abundance values. Individual rats were assigned as a random effect

F value P-value (α= 0.05) Unbaited Control 1.56 0.21 Scarabaeidae 9.61 0.002 ** Dwellers 0.36 0.55 Tunnellers 5.33 0.02 * Rollers 6.58 0.01 * Silphidae 18.68 0.00002 ***

Dung Beetle Phenology May 2016-May 2017 8000

7000

6000

5000

4000

3000 Dung Beetle DungBeetle Abundance 2000

1000

Dwellers Tunnellers Rollers

FIGURE 9. Dung beetle phenology. Data organized by guilds. Abundances provided for every collection period of study across a full calendar year.

Carrion Beetle Phenology May 2016-May 2017 1000

900

800

700

600

500

400

300 Carrion Beetle CarrionBeetle Abundance

200

100

FIGURE 10. Carrion beetle phenology. Abundances provided for every collection period of study across a full calendar year.

TABLE 7. Abiotic factors. Recorded across site and habitat for a full calendar year with averages by season and overall. Seasons were determined by solstice (summer and winter) and equinox (spring and fall) events (National Weather Service 2018).

Maximum Minimum Median Mean Summer 2016 Soil surface temperature (°C) 49.30 19.90 28.70 29.92 Soil surface humidity (%) 96.00 21.00 60.00 59.28 Average wind speed (m/s) 3.60 0.00 1.50 1.81 Light penetration (µmol m-2 s-1) 2211.67 4.00 455.00 738.49 Fall 2016 Soil surface temperature (°C) 33.30 10.40 21.60 20.58 Soil surface humidity (%) 90.00 21.00 70.00 67.70 Average wind speed (m/s) 5.90 0.00 0.50 1.03 Light penetration (µmol m-2 s-1) 1709.67 7.33 319.33 433.36 Winter 2017 Soil surface temperature (°C) 28.00 -4.40 2.90 3.49 Soil surface humidity (%) 66.00 0.00 45.00 39.44 Average wind speed (m/s) 7.70 0.00 1.10 1.58 Light penetration (µmol m-2 s-1) 1284.33 85.67 252.17 367.19 Spring 2017 Soil surface temperature (°C) 26.70 3.40 15.10 15.89 Soil surface humidity (%) 88.00 21.00 64.50 54.34 Average wind speed (m/s) 7.30 0.00 2.85 3.26 Light penetration (µmol m-2 s-1) 1724.67 46.00 365.33 537.47 Overall Soil surface temperature (°C) 49.30 -4.40 20.40 18.56 Soil surface humidity (%) 96.00 0.00 58.00 55.55 Average wind speed (m/s) 7.70 0.00 0.90 1.33 Light penetration (µmol m-2 s-1) 2211.67 4.00 333.33 538.35

CHAPTER 4

DISCUSSION

4.1 Discussion

Based on the clear separation of most natural orifices of the mammalian body at the frontal, or head-end, region and the location of the gastrointestinal tract at the caudal, or tail-end, as well as the presumed preference of carrion feeders to target the head-end and dung feeders the tail-end, we predicted that if dung beetles are attracted to carrion due to the exposure of gut contents through the course of decomposition, then they will be more abundant at the tail-end of a rat carcass. The abundances of dung beetles at the head- and tail-end of rat carrion were different. Results showed that on average, dung beetles were more abundant at the head-end of rat carrion than the tail-end (Figure 7), and the effect of head and tail position of pitfall traps significantly influenced differences in abundance at carrion-baited traps (Table 6). There was no such influence detected at unbaited control points, indicating that the presence of carrion is attractive to dung beetles and that the head-end is preferred in comparison to the tail-end. The preference for head-end assembly at rat carrion suggests that dung is not being targeted as much as carrion itself.

No previous studies have explored head or tail preference of dung beetles at a carcass, but many studies have found that dung beetles are well-represented at carrion-baited traps (Howden and Nealis 1975; Midgley et al. 2012; Ratcliffe 2013) even in temperate regions (Payne 1965;

Ratcliffe and Paulsen 2008; Nadeau et al. 2015) despite the occurrence of dung beetles on carrion outside of the tropics being dismissed as infrequent and insignificant (Halffter and

Matthews 1966). The total abundance of dung beetle individuals collected at rat carrion-baited traps for our year-long study was higher or comparable to North American studies surveying

35 dung beetles with dung-baited traps when accounting for overall sampling efforts (Price 2004;

Bertone et al. 2005; Price et al. 2012; Whipple and Hoback 2012), indicating that carrion is as attractive, if not more attractive, than dung to dung beetles in North America.

A potential confounding factor that we addressed in our experimental design was the effect of wind current direction. It is well-established that the locating of food sources is accomplished by flying into wind currents carrying odor cues for both dung beetles (Halffter and

Matthews 1966) and carrion beetles (Petruska 1975). The predominating winds of the middle division of Kansas (wherein all study sites are located) are from the south between April-October and from the north or northwest between December-March (Kansas Agricultural Experiment

Station 1942). By uniformly orienting the head towards the west and the tail towards the east for every rat carcass across each site, transect, and deployment event, we ensured that the wind current direction and rat carrion orientation were perpendicular for the majority of the year. This limited the potential for wind to cross over the carcass in such a way to carry both head and tail odor cues in the same current. The tradeoff of this decision was that we could not randomize head and tail positioning of rat carcasses along our transects, which would offer some utility in disentangling beetle targeting due to head and tail orientation rather than beetle targeting due to other variables of the landscape. Future studies should consider this tradeoff in their design.

In order to test the assertion that carrion-feeding insects prefer the head region of carcasses, we investigated carrion beetle distribution on rat carrion. We hypothesized that carrion beetles would be more highly represented at the head-end than at the tail-end. Our results show that average carrion beetle abundance is higher at the head-end than at the tail-end (Figure 7), and the head or tail position significantly affects carrion beetle abundance (Table 6). In addition to finding that necrophagous insects preferentially target the head region overall, documentation

36 of carrion beetle distribution at the head- and tail-end of rat carrion is valuable in use as a comparison of distribution patterns for a carrion-targeting beetle group with the distribution of dung beetles, a taxon that may be targeting dung or carrion. We found that both groups, carrion beetles and dung beetles, exhibit an overall pattern of higher representation of individuals at the head-end than at the tail-end of rat carrion. This similar pattern of distribution would suggest that both groups target carrion resources preferentially, challenging commonly held ideas about the role of the temperate dung beetle in decomposing carrion.

In analyzing our abundance data, we also asked the question: does dung beetle abundance differ at the head and tail when the data are categorized into dung beetle behavioral guilds? We found that for roller and tunneller guilds, head or tail position had a significant effect on abundance (Table 6) and observed both guilds having a similar distribution pattern on rat carrion as dung beetles as a whole—a higher abundance at the head-end than at the tail-end, showing a preference for the head and the carrion resources therein (Figure 8). For the dweller guild, no such effect of head and tail position on abundance could be detected, indicating that dwellers do not show a preference for the head- or tail-end (Table 6). The spectrum of functional dung beetle behavior can be arranged on a continuum of less sophisticated behavior, represented most by dwellers, to more sophisticated behavior, represented by rollers (Hanski and Cambefort 1991).

This finding reveals a division among the behavioral guilds in the resources targeted on carrion and is suggestive of another instance of resource partitioning within the dung beetle group with carrion utilization being a more derived, sophisticated feeding behavior.

While most of our questions of beetle preference come down to an analysis of abundances, abundance values alone do not necessarily portray an accurate characterization of the beetle communities found at the head and tail of rat carrion. In order to gain a better understanding of the

37 diversities within these communities, we obtained richness values, evenness values, Shannon-

Wiener diversity indices, and effective species numbers for dung beetles and carrion beetles at both the head- and tail-end of rat carrion. Our results showed that diversity metrics are different for dung beetles compared to carrion beetles, which is not surprising. Dung beetles are a more diverse and abundant group than carrion beetles (Ratcliffe 1996; Ratcliffe and Paulsen 2008). This fact was reflected in diversity metric comparisons of our research as well but is more indicative of each group’s unique evolutionary history than carrion being a more attractive resource to one group over another. Within each group, diversity metrics are similar at the head- and tail-end of rat carrion, suggesting that the resources occurring at the head- and tail-end are not driving differences in community assemblage of either group for any diversity metric beyond abundance.

Lastly, we examined the seasonality of dung beetles and carrion beetles for the duration of our year-long study in order to identify differences in seasonal activity between the two taxa

(Figures 9-10). In temperate regions, most carrion field research takes place only during the warmest times of the year (Benbow et al. 2016), carrying out our field research for a full year put us in a unique position to be able to provide a baseline of phenological data for dung beetles and carrion beetles in the Kansas Flint Hills ecoregion. Phenologies for both taxa are not well- documented. It is important to note that the lack of replication in seasonal data (i.e. multiple years of seasonal data) does not allow us to make clear predictions about seasonal trends of these taxa.

It does, however, allow us to describe dung beetle and carrion beetle seasonality for the year in which this study occurred.

We found that dung beetles dominated every collection period except from February 4 –

April 1, 2017 (collection periods 10 & 11)(Table 2). The highest abundance of dung beetles collected occurred June 25 – August 20, 2016 (collection periods 2 &3) with both collection events

38 yielding more than 8,000 dung beetle individuals. The highest abundance of carrion beetles collected occurred in our first collection event (May 28 – June 25, 2016) and yielded 860 individuals. We found that while dung beetles were collected in overwhelmingly higher numbers, after the winter season carrion beetles became active in higher numbers earlier in the year; from

February 4 – April 1, 2017 (collection periods 10 & 11), carrion beetle abundance highly exceeded dung beetle abundance with only 5 dung beetle individuals compared to 506 carrion beetle individuals collected in collection period 10, and 25 dung beetle individuals compared to 596 carrion beetle individuals collected in collection period 11. This early-year head start observed in carrion beetles is evidence of temporal segregation and suggests a possible mechanism of interspecific coexistence (Kronfeld-Schor and Dayan 1999; Feer and Pincebourde 2005) driven by competition with dung beetles for carrion resources.

The phenology of dung beetle dweller species, Pseudataenius socialis Brown, was of note.

This species is very poorly known in the available literature, in fact “nothing is known of the life history of these beetles other than they are attracted to lights” (Ratcliffe and Paulsen 2008). We established that this species is also attracted to carrion, and we additionally observed that P. socialis exhibits a unique seasonality. The abundance of this species was found to explode during the second collection period (June 25 – July 23, 2016) to 2,075 individuals, an order of magnitude higher than any other dweller species at any point during the year and two orders of magnitude higher than any other occurrence of P. socialis. This drastic appearance and disappearance of P. socialis skews the overall dweller phenology (Figure 9). Aphodius bicolor Say, the second most abundant dweller species after P. socialis, also has a life history that is virtually unknown except for its attraction to human and herbivore dung (Ratcliffe and Paulsen 2008). Other species collected in our carrion-baited traps that were not yet documented at carrion in recent literature

39 include C. fricator, O. knausi, O. orpheus pseudorpheus, P. vindex, C. pilularius, A. erraticus, A. lividus, A. pseudolividus, A. rusicola, A. terminalis, A. spretulus, and A. strigatus (Ratcliffe and

Paulsen 2008).

The exclosure design utilized in this study potentially excluded carrion-attracted insects over 1 cm in diameter. Given the locality in which this study occurred, the only suspected taxon that was likely excluded due to its large size was Dichotomius carolinus (Linnaeus). Dichotomius carolinus, a tunneller dung beetle, was not collected at any carrion-baited traps for the duration of the study, this may have been due to having no attraction to carrion as a resource or, more likely, due to the inability to fit through the 1 cm x 1 cm wire mesh exclosures. Wire exclosures were implemented in an attempt to prevent vertebrate scavenging, and while it may have averted thievery for many passers-by, some enterprising animals were able to bypass our security measures. When rat carrion was suspected of being stolen at a point along the transect, the pit fall trap sample was not included in our data analysis in order to only consider insects that we could confidently assert were attracted to the presence of carrion. A total of 62 rats were stolen out of the 468 rats deployed. All instances of carrion bait thievery occurred from December 2016 – May

2017 and likely skewed beetle abundances in the spring of 2017.

4.2 Significance

Although it is well-established that dung beetles are attracted to carrion, no studies at this time have explored what specific food source (dung or decomposing flesh) dung beetles target on a decomposing carcass. By addressing this gap in research, we increase our understanding of the feeding strategies of dung beetles as well as how they contribute to the recycling of nutrients in an ecosystem. Beetles that interact with carrion receive little attention compared to flies; the few beetle families included in carcass decomposition studies typically include Silphidae,

Staphylinidae, Histeridae, and Dermestidae (Nadeau et al. 2015). Scarabaeidae is frequently dismissed as unimportant to the carrion decomposition process. This research establishes a framework for investigating the contributions of dung beetles to the decomposition process and makes clear that, even in temperate zones, dung beetle interactions with carrion are more complex than previously understood. This research will also contribute to carrion ecology studies by providing a repeatable and statistically sound protocol that can be applied to various other spatial and temporal treatments for future research. Our results challenge current ideas regarding dung beetle contributions to decomposition and shed light on a component of dung beetle ecology that requires more investigation.

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APPENDICES

APPENDIX A

TABLE A: Year-long abundance data for dung beetles at the head- and tail-end of rat carrion at every carrion-baited point along transects Sites= EDSP: “El Dorado State Park”, Eighty: “The 80 Acre”, SARF: “Skeleton Acres Research Facility” Habitat= G: “Grassland”, W: “Woodland” RatID Date Site Point Habitat Head Tail May16ED2G 6/25/2016 EDSP 2 G 3 2 May16ED3G 6/25/2016 EDSP 3 G 1 11 May16ED4G 6/25/2016 EDSP 4 G 13 4 May16ED5G 6/25/2016 EDSP 5 G 4 5 May16ED6G 6/25/2016 EDSP 6 G 5 3 May16ED7G 6/25/2016 EDSP 7 G 23 0 May16ED2W 6/25/2016 EDSP 2 W 6 6 May16ED3W 6/25/2016 EDSP 3 W 18 10 May16ED4W 6/25/2016 EDSP 4 W 2 2 May16ED5W 6/25/2016 EDSP 5 W 2 1 May16ED6W 6/25/2016 EDSP 6 W 2 1 May16ED7W 6/25/2016 EDSP 7 W 4 0 May16EI2G 6/25/2016 Eighty 2 G 15 39 May16EI3G 6/25/2016 Eighty 3 G 146 59 May16EI4G 6/25/2016 Eighty 4 G 27 61 May16EI5G 6/25/2016 Eighty 5 G 186 75 May16EI6G 6/25/2016 Eighty 6 G 11 14 May16EI7G 6/25/2016 Eighty 7 G 16 41 May16EI2W 6/25/2016 Eighty 2 W 1 0 May16EI3W 6/25/2016 Eighty 3 W 4 7 May16EI4W 6/25/2016 Eighty 4 W 18 0 May16EI5W 6/25/2016 Eighty 5 W 20 4 May16EI6W 6/25/2016 Eighty 6 W 0 1 May16EI7W 6/25/2016 Eighty 7 W 13 25 May16SA2G 6/25/2016 SARF 2 G 17 66 May16SA3G 6/25/2016 SARF 3 G 0 0 May16SA4G 6/25/2016 SARF 4 G 0 0 May16SA5G 6/25/2016 SARF 5 G 0 0 May16SA6G 6/25/2016 SARF 6 G 145 144 May16SA7G 6/25/2016 SARF 7 G 256 39 May16SA2W 6/25/2016 SARF 2 W 1 0 May16SA3W 6/25/2016 SARF 3 W 0 4 May16SA4W 6/25/2016 SARF 4 W 2 10 May16SA5W 6/25/2016 SARF 5 W 0 1

RatID Date Site Point Habitat Head Tail May16SA6W 6/25/2016 SARF 6 W 0 6 May16SA7W 6/25/2016 SARF 7 W 23 9 Jun16ED2G 7/23/2016 EDSP 2 G 4 23 Jun16ED3G 7/23/2016 EDSP 3 G 345 121 Jun16ED4G 7/23/2016 EDSP 4 G 68 3 Jun16ED5G 7/23/2016 EDSP 5 G 1 0 Jun16ED6G 7/23/2016 EDSP 6 G 0 6 Jun16ED7G 7/23/2016 EDSP 7 G 11 1 Jun16ED2W 7/23/2016 EDSP 2 W 11 12 Jun16ED3W 7/23/2016 EDSP 3 W 6 7 Jun16ED4W 7/23/2016 EDSP 4 W 1 4 Jun16ED5W 7/23/2016 EDSP 5 W 0 0 Jun16ED6W 7/23/2016 EDSP 6 W 143 7 Jun16ED7W 7/23/2016 EDSP 7 W 7 1 Jun16EI2G 7/23/2016 Eighty 2 G 91 65 Jun16EI3G 7/23/2016 Eighty 3 G 115 41 Jun16EI4G 7/23/2016 Eighty 4 G 48 112 Jun16EI5G 7/23/2016 Eighty 5 G 80 79 Jun16EI6G 7/23/2016 Eighty 6 G 19 16 Jun16EI7G 7/23/2016 Eighty 7 G 200 38 Jun16EI2W 7/23/2016 Eighty 2 W 219 110 Jun16EI3W 7/23/2016 Eighty 3 W 84 11 Jun16EI4W 7/23/2016 Eighty 4 W 99 8 Jun16EI5W 7/23/2016 Eighty 5 W 29 84 Jun16EI6W 7/23/2016 Eighty 6 W 21 14 Jun16EI7W 7/23/2016 Eighty 7 W 13 38 Jun16SA2G 7/23/2016 SARF 2 G 121 176 Jun16SA3G 7/23/2016 SARF 3 G 279 3 Jun16SA4G 7/23/2016 SARF 4 G 0 32 Jun16SA5G 7/23/2016 SARF 5 G 102 19 Jun16SA6G 7/23/2016 SARF 6 G 0 294 Jun16SA7G 7/23/2016 SARF 7 G 531 101 Jun16SA2W 7/23/2016 SARF 2 W 0 0 Jun16SA3W 7/23/2016 SARF 3 W 5 51 Jun16SA4W 7/23/2016 SARF 4 W 11 27 Jun16SA5W 7/23/2016 SARF 5 W 33 0 Jun16SA6W 7/23/2016 SARF 6 W 87 88 Jun16SA7W 7/23/2016 SARF 7 W 115 15 Jul16ED2G 8/20/2016 EDSP 2 G 599 964 Jul16ED3G 8/20/2016 EDSP 3 G 162 164 Jul16ED4G 8/20/2016 EDSP 4 G 33 44 Jul16ED5G 8/20/2016 EDSP 5 G 14 13

RatID Date Site Point Habitat Head Tail Jul16ED6G 8/20/2016 EDSP 6 G 0 0 Jul16ED7G 8/20/2016 EDSP 7 G 75 27 Jul16ED2W 8/20/2016 EDSP 2 W 22 9 Jul16ED3W 8/20/2016 EDSP 3 W 8 14 Jul16ED4W 8/20/2016 EDSP 4 W 10 6 Jul16ED5W 8/20/2016 EDSP 5 W 12 11 Jul16ED6W 8/20/2016 EDSP 6 W 15 10 Jul16ED7W 8/20/2016 EDSP 7 W 3 11 Jul16EI2G 8/20/2016 Eighty 2 G 20 44 Jul16EI3G 8/20/2016 Eighty 3 G 21 145 Jul16EI4G 8/20/2016 Eighty 4 G 176 222 Jul16EI5G 8/20/2016 Eighty 5 G 515 464 Jul16EI6G 8/20/2016 Eighty 6 G 30 38 Jul16EI7G 8/20/2016 Eighty 7 G 145 177 Jul16EI2W 8/20/2016 Eighty 2 W 164 30 Jul16EI3W 8/20/2016 Eighty 3 W 100 2 Jul16EI4W 8/20/2016 Eighty 4 W 50 81 Jul16EI5W 8/20/2016 Eighty 5 W 417 62 Jul16EI6W 8/20/2016 Eighty 6 W 21 55 Jul16EI7W 8/20/2016 Eighty 7 W 59 73 Jul16SA2G 8/20/2016 SARF 2 G 320 233 Jul16SA3G 8/20/2016 SARF 3 G 221 99 Jul16SA4G 8/20/2016 SARF 4 G 24 45 Jul16SA5G 8/20/2016 SARF 5 G 142 151 Jul16SA6G 8/20/2016 SARF 6 G 112 88 Jul16SA7G 8/20/2016 SARF 7 G 156 60 Jul16SA2W 8/20/2016 SARF 2 W 52 33 Jul16SA3W 8/20/2016 SARF 3 W 5 30 Jul16SA4W 8/20/2016 SARF 4 W 27 5 Jul16SA5W 8/20/2016 SARF 5 W 4 19 Jul16SA6W 8/20/2016 SARF 6 W 15 23 Jul16SA7W 8/20/2016 SARF 7 W 31 25 Aug16ED2G 9/17/2016 EDSP 2 G 45 10 Aug16ED3G 9/17/2016 EDSP 3 G 21 17 Aug16ED4G 9/17/2016 EDSP 4 G 82 3 Aug16ED5G 9/17/2016 EDSP 5 G 12 1 Aug16ED6G 9/17/2016 EDSP 6 G 3 10 Aug16ED7G 9/17/2016 EDSP 7 G 2 4 Aug16ED2W 9/17/2016 EDSP 2 W 142 29 Aug16ED3W 9/17/2016 EDSP 3 W 26 10 Aug16ED4W 9/17/2016 EDSP 4 W 5 6 Aug16ED5W 9/17/2016 EDSP 5 W 14 5

RatID Date Site Point Habitat Head Tail Aug16ED6W 9/17/2016 EDSP 6 W 14 4 Aug16ED7W 9/17/2016 EDSP 7 W 8 8 Aug16EI2G 9/17/2016 Eighty 2 G 39 161 Aug16EI3G 9/17/2016 Eighty 3 G 230 0 Aug16EI4G 9/17/2016 Eighty 4 G 125 132 Aug16EI5G 9/17/2016 Eighty 5 G 330 140 Aug16EI6G 9/17/2016 Eighty 6 G 0 25 Aug16EI7G 9/17/2016 Eighty 7 G 373 330 Aug16EI2W 9/17/2016 Eighty 2 W 187 49 Aug16EI3W 9/17/2016 Eighty 3 W 267 29 Aug16EI4W 9/17/2016 Eighty 4 W 159 99 Aug16EI5W 9/17/2016 Eighty 5 W 320 35 Aug16EI6W 9/17/2016 Eighty 6 W 89 27 Aug16EI7W 9/17/2016 Eighty 7 W 76 377 Aug16SA2G 9/17/2016 SARF 2 G 567 8 Aug16SA3G 9/17/2016 SARF 3 G 358 120 Aug16SA4G 9/17/2016 SARF 4 G 66 100 Aug16SA5G 9/17/2016 SARF 5 G 389 312 Aug16SA6G 9/17/2016 SARF 6 G 147 191 Aug16SA7G 9/17/2016 SARF 7 G 182 157 Aug16SA2W 9/17/2016 SARF 2 W 0 68 Aug16SA3W 9/17/2016 SARF 3 W 23 116 Aug16SA4W 9/17/2016 SARF 4 W 70 48 Aug16SA5W 9/17/2016 SARF 5 W 36 77 Aug16SA6W 9/17/2016 SARF 6 W 54 97 Aug16SA7W 9/17/2016 SARF 7 W 95 55 Sep16ED2G 10/15/2016 EDSP 2 G 115 0 Sep16ED3G 10/15/2016 EDSP 3 G 40 4 Sep16ED4G 10/15/2016 EDSP 4 G 67 5 Sep16ED5G 10/15/2016 EDSP 5 G 9 11 Sep16ED6G 10/15/2016 EDSP 6 G 3 8 Sep16ED7G 10/15/2016 EDSP 7 G 7 0 Sep16ED2W 10/15/2016 EDSP 2 W 17 2 Sep16ED3W 10/15/2016 EDSP 3 W 12 12 Sep16ED4W 10/15/2016 EDSP 4 W 6 8 Sep16ED5W 10/15/2016 EDSP 5 W 7 4 Sep16ED6W 10/15/2016 EDSP 6 W 2 7 Sep16ED7W 10/15/2016 EDSP 7 W 0 5 Sep16EI2G 10/15/2016 Eighty 2 G 34 97 Sep16EI3G 10/15/2016 Eighty 3 G 101 20 Sep16EI4G 10/15/2016 Eighty 4 G 1 81 Sep16EI5G 10/15/2016 Eighty 5 G 0 61

RatID Date Site Point Habitat Head Tail Sep16EI6G 10/15/2016 Eighty 6 G 11 25 Sep16EI7G 10/15/2016 Eighty 7 G 0 54 Sep16EI2W 10/15/2016 Eighty 2 W 16 11 Sep16EI3W 10/15/2016 Eighty 3 W 32 23 Sep16EI4W 10/15/2016 Eighty 4 W 100 4 Sep16EI5W 10/15/2016 Eighty 5 W 49 6 Sep16EI6W 10/15/2016 Eighty 6 W 36 8 Sep16EI7W 10/15/2016 Eighty 7 W 28 62 Sep16SA2G 10/15/2016 SARF 2 G 232 181 Sep16SA3G 10/15/2016 SARF 3 G 59 57 Sep16SA4G 10/15/2016 SARF 4 G 17 13 Sep16SA5G 10/15/2016 SARF 5 G 98 43 Sep16SA6G 10/15/2016 SARF 6 G 10 15 Sep16SA7G 10/15/2016 SARF 7 G 127 17 Sep16SA2W 10/15/2016 SARF 2 W 22 26 Sep16SA3W 10/15/2016 SARF 3 W 26 101 Sep16SA4W 10/15/2016 SARF 4 W 17 54 Sep16SA5W 10/15/2016 SARF 5 W 23 36 Sep16SA6W 10/15/2016 SARF 6 W 35 24 Sep16SA7W 10/15/2016 SARF 7 W 60 21 Oct16ED2G 11/12/2016 EDSP 2 G 11 3 Oct16ED3G 11/12/2016 EDSP 3 G 1 7 Oct16ED4G 11/12/2016 EDSP 4 G 22 0 Oct16ED5G 11/12/2016 EDSP 5 G 0 3 Oct16ED6G 11/12/2016 EDSP 6 G 1 0 Oct16ED7G 11/12/2016 EDSP 7 G 8 2 Oct16ED2W 11/12/2016 EDSP 2 W 1 2 Oct16ED3W 11/12/2016 EDSP 3 W 6 6 Oct16ED4W 11/12/2016 EDSP 4 W 2 3 Oct16ED5W 11/12/2016 EDSP 5 W 4 11 Oct16ED6W 11/12/2016 EDSP 6 W 8 5 Oct16ED7W 11/12/2016 EDSP 7 W 0 12 Oct16EI2G 11/12/2016 Eighty 2 G 2 2 Oct16EI3G 11/12/2016 Eighty 3 G 4 0 Oct16EI4G 11/12/2016 Eighty 4 G 12 26 Oct16EI5G 11/12/2016 Eighty 5 G 4 1 Oct16EI6G 11/12/2016 Eighty 6 G 4 12 Oct16EI7G 11/12/2016 Eighty 7 G 2 10 Oct16EI2W 11/12/2016 Eighty 2 W 12 5 Oct16EI3W 11/12/2016 Eighty 3 W 18 3 Oct16EI4W 11/12/2016 Eighty 4 W 65 19 Oct16EI5W 11/12/2016 Eighty 5 W 30 9

RatID Date Site Point Habitat Head Tail Oct16EI6W 11/12/2016 Eighty 6 W 61 3 Oct16EI7W 11/12/2016 Eighty 7 W 31 21 Oct16SA2G 11/12/2016 SARF 2 G 60 58 Oct16SA3G 11/12/2016 SARF 3 G 3 0 Oct16SA4G 11/12/2016 SARF 4 G 1 8 Oct16SA5G 11/12/2016 SARF 5 G 16 1 Oct16SA6G 11/12/2016 SARF 6 G 3 2 Oct16SA7G 11/12/2016 SARF 7 G 0 1 Oct16SA2W 11/12/2016 SARF 2 W 16 49 Oct16SA3W 11/12/2016 SARF 3 W 3 57 Oct16SA4W 11/12/2016 SARF 4 W 5 20 Oct16SA5W 11/12/2016 SARF 5 W 12 6 Oct16SA6W 11/12/2016 SARF 6 W 13 8 Oct16SA7W 11/12/2016 SARF 7 W 84 15 Nov16ED2G 12/10/2016 EDSP 2 G 3 3 Nov16ED3G 12/10/2016 EDSP 3 G 0 1 Nov16ED4G 12/10/2016 EDSP 4 G 0 0 Nov16ED5G 12/10/2016 EDSP 5 G 0 0 Nov16ED6G 12/10/2016 EDSP 6 G 2 0 Nov16ED7G 12/10/2016 EDSP 7 G 3 0 Nov16ED2W 12/10/2016 EDSP 2 W 0 0 Nov16ED3W 12/10/2016 EDSP 3 W 2 4 Nov16ED4W 12/10/2016 EDSP 4 W 0 0 Nov16ED5W 12/10/2016 EDSP 5 W 0 1 Nov16ED6W 12/10/2016 EDSP 6 W 0 0 Nov16ED7W 12/10/2016 EDSP 7 W 2 1 Nov16EI2G 12/10/2016 Eighty 2 G 1 4 Nov16EI3G 12/10/2016 Eighty 3 G 0 0 Nov16EI4G 12/10/2016 Eighty 4 G 1 1 Nov16EI5G 12/10/2016 Eighty 5 G 0 0 Nov16EI6G 12/10/2016 Eighty 6 G 1 0 Nov16EI7G 12/10/2016 Eighty 7 G 0 1 Nov16EI2W 12/10/2016 Eighty 2 W 11 3 Nov16EI3W 12/10/2016 Eighty 3 W 14 4 Nov16EI4W 12/10/2016 Eighty 4 W 9 3 Nov16EI5W 12/10/2016 Eighty 5 W 9 2 Nov16EI6W 12/10/2016 Eighty 6 W 2 1 Nov16EI7W 12/10/2016 Eighty 7 W 18 25 Nov16SA2G 12/10/2016 SARF 2 G 4 9 Nov16SA3G 12/10/2016 SARF 3 G 0 0 Nov16SA4G 12/10/2016 SARF 4 G 1 1 Nov16SA5G 12/10/2016 SARF 5 G 2 0

RatID Date Site Point Habitat Head Tail Nov16SA6G 12/10/2016 SARF 6 G 1 0 Nov16SA7G 12/10/2016 SARF 7 G 2 3 Nov16SA2W 12/10/2016 SARF 2 W 15 19 Nov16SA3W 12/10/2016 SARF 3 W 4 21 Nov16SA4W 12/10/2016 SARF 4 W 7 11 Nov16SA5W 12/10/2016 SARF 5 W 4 2 Nov16SA6W 12/10/2016 SARF 6 W 7 12 Nov16SA7W 12/10/2016 SARF 7 W 89 8 Dec16ED2G 1/7/2017 EDSP 2 G 0 0 Dec16ED3G 1/7/2017 EDSP 3 G 0 0 Dec16ED4G 1/7/2017 EDSP 4 G 0 0 Dec16ED5G 1/7/2017 EDSP 5 G 0 0 Dec16ED6G 1/7/2017 EDSP 6 G 0 0 Dec16ED7G 1/7/2017 EDSP 7 G 0 0 Dec16ED2W 1/7/2017 EDSP 2 W 0 0 Dec16ED3W 1/7/2017 EDSP 3 W 0 1 Dec16ED4W 1/7/2017 EDSP 4 W 0 0 Dec16ED5W 1/7/2017 EDSP 5 W 0 1 Dec16ED6W 1/7/2017 EDSP 6 W 0 0 Dec16ED7W 1/7/2017 EDSP 7 W 0 0 Dec16EI2G 1/7/2017 Eighty 2 G 0 0 Dec16EI3G 1/7/2017 Eighty 3 G 0 0 Dec16EI4G 1/7/2017 Eighty 4 G 0 0 Dec16EI5G 1/7/2017 Eighty 5 G 0 0 Dec16EI6G 1/7/2017 Eighty 6 G 0 0 Dec16EI7G 1/7/2017 Eighty 7 G 0 0 Dec16EI2W 1/7/2017 Eighty 2 W 1 0 Dec16EI3W 1/7/2017 Eighty 3 W 1 6 Dec16EI4W 1/7/2017 Eighty 4 W 3 0 Dec16EI5W 1/7/2017 Eighty 5 W 3 1 Dec16EI6W 1/7/2017 Eighty 6 W 5 0 Dec16EI7W 1/7/2017 Eighty 7 W 0 4 Dec16SA2G 1/7/2017 SARF 2 G 0 0 Dec16SA3G 1/7/2017 SARF 3 G 0 0 Dec16SA4G 1/7/2017 SARF 4 G 0 0 Dec16SA7G 1/7/2017 SARF 7 G 1 0 Dec16SA2W 1/7/2017 SARF 2 W 2 5 Dec16SA3W 1/7/2017 SARF 3 W 0 5 Dec16SA4W 1/7/2017 SARF 4 W 1 0 Dec16SA5W 1/7/2017 SARF 5 W 2 2 Dec16SA6W 1/7/2017 SARF 6 W 2 0 Dec16SA7W 1/7/2017 SARF 7 W 3 2

RatID Date Site Point Habitat Head Tail Jan17ED2G 2/4/2017 EDSP 2 G 0 0 Jan17ED4G 2/4/2017 EDSP 4 G 0 0 Jan17ED6G 2/4/2017 EDSP 6 G 2 0 Jan17ED2W 2/4/2017 EDSP 2 W 0 0 Jan17ED3W 2/4/2017 EDSP 3 W 0 0 Jan17ED4W 2/4/2017 EDSP 4 W 0 0 Jan17ED5W 2/4/2017 EDSP 5 W 0 0 Jan17ED6W 2/4/2017 EDSP 6 W 0 0 Jan17ED7W 2/4/2017 EDSP 7 W 0 0 Jan17EI2G 2/4/2017 Eighty 2 G 0 1 Jan17EI3G 2/4/2017 Eighty 3 G 0 0 Jan17EI4G 2/4/2017 Eighty 4 G 0 0 Jan17EI5G 2/4/2017 Eighty 5 G 0 0 Jan17EI6G 2/4/2017 Eighty 6 G 0 0 Jan17EI7G 2/4/2017 Eighty 7 G 0 0 Jan17EI2W 2/4/2017 Eighty 2 W 0 0 Jan17EI3W 2/4/2017 Eighty 3 W 0 1 Jan17EI4W 2/4/2017 Eighty 4 W 0 1 Jan17EI5W 2/4/2017 Eighty 5 W 1 0 Jan17EI6W 2/4/2017 Eighty 6 W 0 0 Jan17EI7W 2/4/2017 Eighty 7 W 0 0 Feb17ED2G 3/4/2017 EDSP 2 G 0 0 Feb17ED3G 3/4/2017 EDSP 3 G 0 0 Feb17ED4G 3/4/2017 EDSP 4 G 0 0 Feb17ED5G 3/4/2017 EDSP 5 G 0 0 Feb17ED6G 3/4/2017 EDSP 6 G 0 0 Feb17ED7G 3/4/2017 EDSP 7 G 0 0 Feb17ED2W 3/4/2017 EDSP 2 W 0 0 Feb17ED3W 3/4/2017 EDSP 3 W 0 0 Feb17ED4W 3/4/2017 EDSP 4 W 0 0 Feb17ED5W 3/4/2017 EDSP 5 W 0 0 Feb17ED6W 3/4/2017 EDSP 6 W 0 0 Feb17ED7W 3/4/2017 EDSP 7 W 0 0 Feb17EI2G 3/4/2017 Eighty 2 G 0 0 Feb17EI3G 3/4/2017 Eighty 3 G 0 0 Feb17EI4G 3/4/2017 Eighty 4 G 0 0 Feb17EI5G 3/4/2017 Eighty 5 G 0 0 Feb17EI6G 3/4/2017 Eighty 6 G 1 0 Feb17EI7G 3/4/2017 Eighty 7 G 0 0 Feb17EI2W 3/4/2017 Eighty 2 W 0 0 Feb17EI3W 3/4/2017 Eighty 3 W 0 0 Feb17EI4W 3/4/2017 Eighty 4 W 0 0

RatID Date Site Point Habitat Head Tail Feb17EI5W 3/4/2017 Eighty 5 W 0 0 Feb17EI6W 3/4/2017 Eighty 6 W 0 0 Feb17EI7W 3/4/2017 Eighty 7 W 0 1 Feb17SA4G 3/4/2017 SARF 4 G 0 0 Mar17ED2G 4/1/2017 EDSP 2 G 0 0 Mar17ED3G 4/1/2017 EDSP 3 G 0 0 Mar17ED4G 4/1/2017 EDSP 4 G 0 0 Mar17ED5G 4/1/2017 EDSP 5 G 0 0 Mar17ED6G 4/1/2017 EDSP 6 G 0 0 Mar17ED7G 4/1/2017 EDSP 7 G 0 0 Mar17ED2W 4/1/2017 EDSP 2 W 0 0 Mar17ED3W 4/1/2017 EDSP 3 W 0 0 Mar17ED4W 4/1/2017 EDSP 4 W 0 0 Mar17ED5W 4/1/2017 EDSP 5 W 0 0 Mar17ED6W 4/1/2017 EDSP 6 W 0 0 Mar17ED7W 4/1/2017 EDSP 7 W 0 0 Mar17EI2G 4/1/2017 Eighty 2 G 0 1 Mar17EI3G 4/1/2017 Eighty 3 G 0 0 Mar17EI4G 4/1/2017 Eighty 4 G 0 0 Mar17EI5G 4/1/2017 Eighty 5 G 0 0 Mar17EI6G 4/1/2017 Eighty 6 G 0 0 Mar17EI7G 4/1/2017 Eighty 7 G 0 0 Mar17EI2W 4/1/2017 Eighty 2 W 0 0 Mar17EI3W 4/1/2017 Eighty 3 W 0 0 Mar17EI4W 4/1/2017 Eighty 4 W 0 0 Mar17EI5W 4/1/2017 Eighty 5 W 0 0 Mar17EI6W 4/1/2017 Eighty 6 W 0 0 Mar17EI7W 4/1/2017 Eighty 7 W 0 0 Mar17SA3G 4/1/2017 SARF 3 G 0 0 Mar17SA5W 4/1/2017 SARF 5 W 0 0 Apr17ED2G 5/2/2017 EDSP 2 G 0 0 Apr17ED3G 5/2/2017 EDSP 3 G 0 0 Apr17ED4G 5/2/2017 EDSP 4 G 1 0 Apr17ED5G 5/2/2017 EDSP 5 G 0 0 Apr17ED6G 5/2/2017 EDSP 6 G 0 0 Apr17ED7G 5/2/2017 EDSP 7 G 0 0 Apr17ED2W 5/2/2017 EDSP 2 W 3 0 Apr17ED3W 5/2/2017 EDSP 3 W 0 0 Apr17ED4W 5/2/2017 EDSP 4 W 0 1 Apr17ED5W 5/2/2017 EDSP 5 W 0 0 Apr17ED6W 5/2/2017 EDSP 6 W 0 0 Apr17ED7W 5/2/2017 EDSP 7 W 0 0

RatID Date Site Point Habitat Head Tail Apr17EI2G 5/2/2017 Eighty 2 G 0 0 Apr17EI3G 5/2/2017 Eighty 3 G 1 0 Apr17EI4G 5/2/2017 Eighty 4 G 1 0 Apr17EI5G 5/2/2017 Eighty 5 G 5 1 Apr17EI6G 5/2/2017 Eighty 6 G 0 0 Apr17EI7G 5/2/2017 Eighty 7 G 2 2 Apr17EI2W 5/2/2017 Eighty 2 W 0 1 Apr17EI3W 5/2/2017 Eighty 3 W 0 1 Apr17EI4W 5/2/2017 Eighty 4 W 0 0 Apr17EI5W 5/2/2017 Eighty 5 W 1 0 Apr17EI6W 5/2/2017 Eighty 6 W 0 0 Apr17EI7W 5/2/2017 Eighty 7 W 1 0 May17ED2G 5/27/2017 EDSP 2 G 23 6 May17ED3G 5/27/2017 EDSP 3 G 5 12 May17ED4G 5/27/2017 EDSP 4 G 5 6 May17ED5G 5/27/2017 EDSP 5 G 12 3 May17ED6G 5/27/2017 EDSP 6 G 5 11 May17ED7G 5/27/2017 EDSP 7 G 6 6 May17ED2W 5/27/2017 EDSP 2 W 6 6 May17ED3W 5/27/2017 EDSP 3 W 18 10 May17ED4W 5/27/2017 EDSP 4 W 2 2 May17ED5W 5/27/2017 EDSP 5 W 2 1 May17ED6W 5/27/2017 EDSP 6 W 2 1 May17ED7W 5/27/2017 EDSP 7 W 4 0 May17EI2G 5/28/2017 Eighty 2 G 0 21 May17EI3G 5/28/2017 Eighty 3 G 18 12 May17EI4G 5/28/2017 Eighty 4 G 11 45 May17EI5G 5/28/2017 Eighty 5 G 22 2 May17EI6G 5/28/2017 Eighty 6 G 3 1 May17EI7G 5/28/2017 Eighty 7 G 14 21 May17EI2W 5/28/2017 Eighty 2 W 1 0 May17EI3W 5/28/2017 Eighty 3 W 0 4 May17EI4W 5/28/2017 Eighty 4 W 2 10 May17EI5W 5/28/2017 Eighty 5 W 0 1 May17EI6W 5/28/2017 Eighty 6 W 0 6 May17EI7W 5/28/2017 Eighty 7 W 23 9

APPENDIX B

TABLE B: Abundance data of dung beetle species at the head- and tail-end of rat carrion

Species Guild Head Tail AteuchusHisteroides Tunneller 364 307 OnthophagusHecate Tunneller 3181 1944 OnthophagusPennysylvanicus Tunneller 6513 4508 OnthophagusKnausi Tunneller 603 485 CoprisMinutus Tunneller 633 537 OnthophagusOrpheusPseudorpheus Tunneller 64 59 PhanaeusVindex Tunneller 33 36 CoprisFricator Tunneller 62 60 CanthonPilularius Roller 1382 931 CanthonViridis Roller 161 136 PseudocanthonPerplexus Roller 579 192 AphodiusBicolor Dweller 102 56 PseudataeniusSocialis Dweller 914 1201 AphodiusErraticus Dweller 2 0 AphodiusPseudolividus Dweller 1 8 AphodiusLividus Dweller 0 2 AtaeniusSpretulus Dweller 1 1 AtaeniusStrigatus Dweller 16 10 AphodiusTerminalis Dweller 2 4 AphodiusCarolinus Dweller 0 0 AphodiusFemoralis Dweller 1 2 AphodiusRusicola Dweller 1 1