Habitat Associations of Coexisting Carrion Beetles (Subfamilies

HABITAT ASSOCIATIONS OF COEXISTING CARRION BEETLES (SUBFAMILIES

NICROPHORINAE AND SILPHINAE) IN SOUTHEASTERN ONTARIO

Kevin William Burke

A thesis submitted to the Department of Biology

in conformity with the requirements for the

degree of Master of Science

Queen’s University

Kingston, Ontario, Canada

September 2019

Abstract

The coexistence of closely related species is thought to play an important role in shaping and maintaining local diversity and community organization. However, competition for shared limiting resources can inhibit coexistence unless species can reduce overlap in resource requirements or minimize differences in competitive ability. Many co-occurring species avoid the costs of coexistence by diverging in habitat use through a process known as habitat partitioning, allowing them to spatially avoid potential competitors. Habitat partitioning appears common among coexisting species and is thought to have important consequences for the evolution of species and traits, and community structure. Yet, despite the commonness of habitat partitioning, little is known about how and when habitat partitioning occurs and its role in facilitating species coexistence. Here, we take the first steps to understanding the role habitat partitioning plays in facilitating coexistence between seven species of burying beetles (genus:

Nicrophorus) by examining their habitat associations where they co-occur. We test the hypothesis that co-occurring Nicrophorus species in southeastern Ontario partition resources by associating with different habitat characteristics or distinct habitat types, potentially to facilitate coexistence. To test this idea, we conducted a large-scale survey of carrion beetle abundance and

54 quantitative habitat characteristics at 100 randomly generated sites spanning an environmentally diverse and heterogenous region of southeastern Ontario. We identified the habitat associations of six co-occurring Nicrophorus species and three other carrion beetle species in the subfamily Silphinae. Our findings indicate that co-occurring Nicrophorus species do differ in their habitat use in a pattern consistent with habitat partitioning. Specifically, three

Nicrophorus species (Nicrophorus pustulatus, N. hebes, and N. marginatus) were found to be habitat specialists for the forest canopy, wetlands, and open fields, respectively. Three other iii

Nicrophorus species (N. orbicollis, N. sayi, and N. tomentosus) were found to be habitat generalists with wider breadths of habitat use and high overlap in habitat use with some other species. Our findings suggest that habitat may be an important resource axis along which some

Nicrophorus species partition, however, divergence along other resource axes is likely also important for facilitating Nicrophorus coexistence.

Acknowledgments

Foremost, I’d like to thank my supervisor Dr. Paul R. Martin for his invaluable guidance, support, and encouragement provided throughout the past two years. Thank you for always fostering my ambitions and providing so many opportunities to try different projects, learn new skills, and to become an overall better scientist. I’d also like to thank my committee members Dr.

Frances Bonier and Dr. Chris Eckert for their insightful comments and suggestions. Special thanks to Jillian Wettlaufer, Allison Collard, and all my volunteers for their help collecting data in the field and in the lab. Additional thanks to Jillian Wettlaufer, Jaimie Bortolotti, Sarena

Olsen, Liam Harrison, Haley Kenyon, Adam Groulx, Matthew Macpherson, and the rest of the

Martin and Bonier labs for the friendship, support, and help they’ve provided along the way. I’d also like to thank NSERC, Queen’s University, and the Province of Ontario for providing funding for this research and the Queen’s University Biological Station for providing a place to stay and conduct my research during the summers. Lastly, thank you to my parents, Kim and

Duncan Burke, my extended family, and Sharla Foster for your unending support and unwavering belief in me.

Table of Contents Abstract………………………………………………………………..…………...…………… ii Acknowledgments……………………………………………………………...………………. iv Table of Contents…………………………………………………………..………………….... v List of Figures...……………………………………………………………...…………...…...... vi List of Tables..………………………………………………………………...……………….. vii Chapter 1: General Introduction…………………………………………………………...…. 1 The Paradox of Species Coexistence……………...………………………...…………… 1 Mechanisms of Species Coexistence……………..……………………………..……….. 2 Resource Partitioning……………………..……………...………………………...…….. 5 The Role of Competition in Resource Partitioning………….………………...…………. 6 Habitat Partitioning………………………………………...………………….…………. 8 Coexisting Carrion Beetles in Southeastern Ontario………………..…………..……… 10 Scope of this Thesis……………………………………………….……………...…….. 12 Chapter 2: Methods…………………………………………………………………….……... 14 Site Description………………………………………………………………..…..……. 14 Survey of Carrion Beetle Abundance…………………………………………………... 14 Survey of Local Habitat Characteristics………………………………………………... 16 Ground Cover, Leaf Litter, and Soil Characteristics…………………..….....…. 16 Habitat Type, Tree Species Diversity, and Tree Size ………………....……….. 16 Statistical Analyses…………………………………………………………………...... 17 Conditional Inference Tree Classification……………………………………… 18 Chapter 3: Results……………………………………………………………………..………. 20 Chapter 4: Discussion …………………………………………………………………..…….. 26 Habitat Associations of Nicrophorinae…………………………………………………. 26 Habitat Associations of Silphinae……………………………………………....………. 34 General Patterns of Habitat Use………………………………………………………… 36 Literature Cited………………………………………………………………………….……. 42 Appendix A…………………………………………………………………………………….. 66

List of Figures

Figure 1. Site Map…………………………...…………………………………………………. 15

Figure 2. Conditional inference trees of N. orbicollis and N. tomentosus habitat associations……………………………………………………………………………………... 21

Figure 3. Conditional inference trees of N. sayi habitat associations…………...……………... 22

Figure 4. Conditional inference trees of N. pustulatus, N. marginatus, and N. hebes habitat associations……………………………………………………………………………………... 23

Figure 5. Conditional inference trees of N. defodiens and Necrodes surinamensis habitat associations……………………………………………………………………………………... 24

Figure 6. Conditional inference trees of Necrophila americana, Oiceoptoma inaequale, and O. noveboracense habitat associations…………………………………………………………….. 25

Figure 7. Graphical representation of the habitat associations of Nicrophorus species in southeastern Ontario with molecular phylogeny……………………………………………….. 27

vii

List of Tables

Table 1. Summary of 2017 carrion beetle abundance survey………………...………………... 18

Table S1. Descriptions and abbreviations for all habitat characteristics measured……...... ….. 66

Chapter 1: General Introduction

The Paradox of Species Coexistence

What processes are responsible for the generation and maintenance of the diversity of life? This question lies at the heart of all biology, yet, after centuries of research, universal answers that extend across environments and taxa remain elusive (Lawton 1999; Simberloff

2004; Vellend 2016). Of particular interest to ecologists is understanding how species with similar ecologies and resource requirements coexist within biological communities and how the coexistence of these species influences local diversity (Hutchinson 1959, 1961; Tilman 1982;

Chesson 2000). The coexistence of ecologically similar species is paradoxical because traditional ecological theory predicts that competition for shared resources should cause all but one or a few of these species to be excluded from a community (Gause 1932; Hardin 1960; Violle et al. 2011).

Contrary to these ideas, however, coexisting ecologically similar species are thought to make up a large component of local diversity and the interactions between them can influence community organization and composition (Toft 1985; Wright 2002; Siepielski and McPeek 2010; Burns and

Strauss 2011). Therefore, understanding how and when species coexist is crucial for our understanding of how local diversity is structured and maintained.

Coexistence is especially problematic for closely related species due to their high degree of ecological similarity inherited from a recent common ancestor (Richman and Price 1992;

Burns and Strauss 2011). Accordingly, closely related species exhibit high overlap in resource requirements resulting in more intense competition between closely related species than with more distantly related species (MacArthur and Levins 1967; Abrams 1983; Burns and Strauss

2011; Violle et al. 2011). Despite this competition, closely related species from a wide range of taxonomic groups do coexist, including amphibians (Inger and Greenberg 1966; Toft 1980, 2

1985; Menin et al. 2005), reptiles (Pianka 1969; James and Shine 2000; Dias and Rocha 2006), insects (Johnson and Hubbell 1975; Strong 1982; Rowe and Berrill 1989; Zhang et al. 2004;

Kadowaki 2010), birds (Diamond 1973; Schmutz et al. 1980; Robinson and Terborgh 1995;

Gómez et al. 2010; Freshwater et al. 2014), mammals (Kotler and Brown 1988; Ziv et al. 1993;

Kingston et al. 2000; Price et al. 2000; Leaver and Daly 2001), fish (Robertson and Gaines 1986;

Genner et al. 1999; Hilton et al. 2008; Ohlberger et al. 2008; Navarro et al. 2009), and plants

(Grace and Wetzel 1981; Rydin and Barber 2001; Wright 2002; Kursar et al. 2009).

Furthermore, the coexistence of closely related species is thought to play an important role in shaping patterns of biodiversity by influencing community structure, the evolution of species traits, and rates of diversification (Brown and Wilson 1956; Richman and Price 1992; Grant and

Grant 2006; Price et al. 2014).

Mechanisms of Species Coexistence

Many theories have been proposed to explain how ecologically similar and closely related species achieve coexistence. Notable contributions include the Lotka and Volterra mathematical models of species population dynamics (Volterra 1926; Lotka 1932; MacArthur

1970), community assembly rules (Diamond 1975; Keddy 1992; Weiher et al. 1998), the theory of island biogeography and its subsequent extensions to continental communities (MacArthur and Wilson 1967; MacArthur 1972; Brown and Lomolino 2000), the ecological niche concept and niche theory (Hutchinson 1957; MacArthur and Levins 1967; Vandermeer 1972; Leibold

1995; Holt 2009), the metacommunity concept (Wilson 1992; Zobel 1997; Mouquet and Loreau

2002; Leibold et al. 2004), the neutral theory of species coexistence (Hubbell 2001, 2005; Chave

2004), and modern coexistence theory (Chesson 2000; Adler et al. 2007; HilleRisLambers et al. 3

2012). Central to many of these theories is the idea that for coexistence to occur, co-occurring species must be able to persist and recover from low abundances when competitor species are at typical abundance levels, thus avoiding local extinction (MacArthur 1972; Chesson 2000). At the local community level, the ability of species to co-occur and meet this requirement is thought to be mediated primarily through species interactions and environmental conditions that act as filters for the kinds of species that can occur within a community (Schoener 1974a, 1983;

Schmitt and Holbrook 2003; Burns and Strauss 2011; Violle et al. 2011; HilleRisLambers et al.

2012; Kraft et al. 2015). Modern coexistence theory attempts to provide a comprehensive framework for understanding how co-occurring species coexist at the local community level

(Chesson 2000). According to modern coexistence theory, coexistence between species is arbitrated by the interactions between two opposing processes: 1) the evolution of competitive differences between species, and 2) stabilizing mechanisms that reduce species interactions and overlap in resource requirements (Chesson 2000).

Differences between co-occurring species that affect the outcome of competition for limiting resources can act to inhibit coexistence by facilitating competitive exclusion (Gause

1932; Hardin 1960; Violle et al. 2011). Competitively superior species inevitably out-compete competitively inferior species for shared resources, resulting in the exclusion of less competitive species from communities. Differences in competitive ability between species can be reduced, or neutralized, through equalizing mechanisms (Chesson 2000). Equalizing mechanisms such as fundamental trade-offs in traits linked directly to resource acquisition and reproduction, or the density-dependent effects of natural enemies, serve to make co-occurring species competitively equivalent (Chesson 2000; Hubbell 2005; Leibold and McPeek 2006; Adler et al. 2007; Martin

2015). In stable environments, competitively equivalent species will be unable to out-compete 4

one another for shared resources (Scheffer et al. 2018). Instead, coexistence and the structure of communities would be regulated by stochastic processes that result in random fluctuations in the populations of co-occurring species (Hubbell 2001, 2005; Leibold and McPeek 2006; Vellend

2010). However, there is currently little empirical evidence of species coexistence driven by neutral differences and random processes, nor might equalizing mechanisms alone be enough to completely negate competitive differences between species (Chesson 2000; McGill et al. 2006;

Vellend 2010). Furthermore, coexistence may be unlikely to be achieved, even in the absence of competitive differences between species without the additional effects of stabilizing mechanisms

(Chesson 2000; HilleRisLambers et al. 2012).

Stabilizing mechanisms are essential for species coexistence and allow co-occurring species to overcome differences in competitive ability by reducing the influence on population growth of interspecific competition relative to intraspecific competition (Chesson 2000;

HilleRisLambers et al. 2012). Stabilizing mechanisms function by creating and reinforcing differences in species’ ecologies and resource use, thereby reducing ecological similarity and reliance on shared resources between species. By differentiating in ecology and resource use, competition between species for shared resources is reduced relative to competition within species. Thus, intra-specific competition becomes a greater determinant of the population dynamics of co-occurring species and this can result in frequency-dependent shifts in population growth rates as populations approach their carrying capacity or local extinction (Chesson 2000).

When a species is abundant, competition for limited resources increases within species, resulting in a reduction in population growth rates and constraining population size as resource availability declines (Chesson 2000; Adler et al. 2007). In contrast, competition within species decreases when abundance is low, resulting in high resource availability and increased population growth 5

rates, enabling species to persist and recover when populations near extinction (Chesson 2000;

HilleRisLambers et al. 2012). Therefore, stabilizing mechanisms facilitate coexistence by reducing interspecific competition, thus allowing intraspecific competition to constrain population growth and buffer co-occuring species against local extinction (Chesson 2000; Adler et al. 2007; HilleRisLambers et al. 2012).

Resource Partitioning

One of the most common and well-studied forms of stabilizing mechanisms is resource partitioning, in which species partition their use of available resources along environmental gradients (Schoener 1968, 1974a, 1986; Ross 1986; Wright 2002). During resource partitioning, co-occurring species diverge in the resources they use or in how they use them, thus reducing overlap in resource requirements and the frequency of competitive interactions (Brown and

Wilson 1956; Schoener 1974a; Losos 1994). Species may partition resources along any characteristic of their environment that spans a gradient, however, time, resource type, and space may be particularly important among coexisting species (Schoener 1974a, 1986; Carothers and

Jaksić 1984). Species can partition time by diverging in diel or seasonal activity, thus avoiding competitors and potentially gaining access to novel time-sensitive or seasonal resources

(Schoener 1974a, 1974b; Ziv et al. 1993; Kronfeld-Schor and Dayan 2003). Species can partition resource types by differentiating in the kinds or sizes of resources they use, for example, by consuming different foods or using distinct nest sites, which can reduce overlap in shared resource requirements (Husar 1976; Ganzhorn 1988; Bootsma et al. 1996; de Mérona and

Rankin-de-Mérona 2004). Finally, species can partition spatially by separating their activity along spatially-distributed environmental gradients or between distinct habitat types (Grace and 6

Wetzel 1981; Arlettaz 1999; Albertson 2008; Hilton et al. 2008). Regardless of the resources being partitioned, resource partitioning is thought to be an essential process for facilitating species coexistence and shaping species composition, distributions, and abundances within communities (Schoener 1974a, 1986; Toft 1985; Wisheu 1998). Understanding how coexisting species use different resources is essential for understanding how and when such species coexist.

The Role of Competition in Resource Partitioning

Despite the importance of resource partitioning for facilitating species coexistence, the mechanisms underlying it remain poorly understood in many systems (Schoener 1982; Connell

1983; Toft 1985; Schluter 2000). Understanding these mechanisms is important in order to identify the conditions where we expect resource partitioning among species, versus the conditions where we expect one species to use all resources to the exclusion of other species.

Previously, interspecific competition was often assumed to be the overriding process shaping patterns of resource partitioning. However, some researchers have questioned the role interspecific competition plays in shaping resource partitioning and species coexistence due to the relative lack of explicit testing of interspecific competitions effects on resource use among co-occurring species (Schoener 1983; Niemelä 1993). Fortunately, contemporary studies have since made great progress in furthering our understanding of the mechanisms of resource partitioning, both expanding our knowledge of the role of interspecific competition and extending our knowledge beyond competition to recognize a variety of alternative mechanisms.

Focused investigations into the processes underlying resource partitioning have revealed that while interspecific competition does frequently occur, it is not the only process capable of 7

producing patterns of differing resource use among co-occurring species (Schoener 1974a;

Connell 1983; Wisheu 1998). Predators, parasites, and diseases that do not discriminate between closely related or similar species can increase mortality for all co-occurring species at higher densities, thus favoring divergence in resource use to avoid population clumping (Freeland 1983;

Holt and Pickering 1985; Martin 1993, 1996, 1988a, 1988b; Kotler et al. 1991; Begon et al.

1992; Abrams 2000; Feener 2000; Chesson and Kuang 2008; Jachowski et al. 2014). Local adaptation can select for species to specialize and exclusively use resources that optimize competitive and reproductive performance, or to evolve to take advantage of novel resources regardless of interspecific competition (Bouton et al. 1999; Leal and Fleishman 2002; Ellis and

Weis 2006; Hereford 2009). Differing dispersal ability between species can differentially limit the local distributions and resources available to co-occurring species (MacArthur 1958;

Diamond 1975; Tilman 1997; Chesson and Snyder 2003). Similarly, pre-existing differences in resource use, evolved in areas where species do not co-occur, if conserved, can yield patterns of resource partitioning where they do co-occur in the absence of the effects of interspecific competition (Leibold et al. 2004; Questad and Foster 2008; Lasky et al. 2013; Kraft et al. 2015).

Lastly, contemporary patterns of resource partitioning can be the legacy of historical interspecific competition that selected for divergence in resource use in the past but is now no longer relevant (Connell 1980; Pritchard and Schluter 2001). These alternative mechanisms highlight that resource partitioning and coexistence can be more complex than previously thought and that experimental testing is needed to determine how and why co-occurring species differ in resource use.

Interspecific competition is still a pervasive and strongly influential process for shaping patterns of resource use and species coexistence. The occurrence of interspecific competition has 8

been documented among many coexisting species and evidence from a variety of experimental studies suggests that it often plays a primary role in organizing communities of similar and closely related species (Connell 1961, 1983; Hairston 1980a; Schoener 1983; Robertson and

Gaines 1986; Freeman 2015). Field and laboratory experiments that manipulate the co- occurrence and abundances of potential competitors to observe responses in fecundity, survivorship, and population size, have been particularly useful for discerning the role of interspecific competition in producing patterns of resource partitioning (Connell 1961; Schoener

1974a, 1983; Hairston 1980a, 1980b; Heske et al. 1994; Stuart et al. 2014). Such studies have revealed that interspecific competition appears to be responsible for patterns of resource partitioning and species coexistence more often among species that share strongly limiting or homogenously distributed resources, or that experience low levels of predation and parasitism

(Connell 1961; Schoener 1983). Additionally, interspecific competition and other mechanisms can act both independently or in combination to produce patterns of resource partitioning and species coexistence (Schoener 1974a, 1983; Connell 1983; Toft 1985; Kotler et al. 1991).

Nonetheless, while differences in resource use are commonly described between co-occurring species, interspecific competition cannot simply be assumed to be responsible, nor can patterns of differential resource use be assumed to exist to facilitate coexistence, without explicit testing of the underlying mechanisms.

Habitat Partitioning

Many coexisting species avoid the costs of coexistence by evolving to occupy different habitats through a process known as habitat partitioning. Habitat partitioning allows similar and closely related species to coexist by spatially separating potential competitors (MacArthur 1958; 9

Grace and Wetzel 1981; Albertson 2008). Habitat partitioning may be common among co- occurring taxa around the world and may be an important early step in species divergence and trait evolution (Schoener 1974a; Toft 1985; Richman and Price 1992; Wisheu 1998; Freeman

2015). Likewise, the extent of habitat partitioning among species may be a primary determinant of the number and types of species that can occur in a community (Kadmon and Allouche 2007).

Among many co-occurring taxa, habitat partitioning is the most common form of resource partitioning, occurring at significantly greater frequencies and producing larger differences in resource use than either the partitioning of time or resource types (Schoener 1974a, 1986; Toft

1985). The prevalence of habitat partitioning may be due to several factors. Foremost, habitat and spatial gradients are widely available and partitionable. Additionally, unlike time or resource type partitioning, habitat partitioning often does not require complex physiological or morphological adaptations to be facilitated, nor does it incur costs to potential energy or resource gain by limiting the kinds of resources species can use or the time they can spend securing them

(Schoener 1974b, 1986). Overall, habitat partitioning appears crucial for facilitating species coexistence, diversification, and community organization.

Despite the apparent ubiquity of habitat partitioning among coexisting species, few general rules have been identified governing how and when habitat partitioning occurs across environments and taxa (Schoener 1974a; Toft 1985). Furthermore, surprisingly little is known about the underlying mechanisms of habitat partitioning or its role in facilitating species coexistence relative to other forms of resource partitioning, such as the partitioning of time or resource types (Wisheu 1998).

Coexisting Carrion Beetles in Southeastern Ontario 10

In southeastern Ontario, seven species of burying beetle (subfamily: Nicrophorinae, genus: Nicrophorus) co-occur despite all requiring a shared, limiting resource for reproduction.

These species include Nicrophorus orbicollis, N. sayi, N. tomentosus, N. pustulatus, N. defodiens, N. hebes (previously N. vespilloides; Sikes et al. 2016), and N. marginatus (Anderson

1982; Anderson and Peck 1985; Beninger and Peck 1992; Robertson 1992). All burying beetle species require the carcasses of small vertebrates for reproduction, which they bury and use as a primary food source and nest for developing larvae (Pukowski 1933; Wilson and Fudge 1984;

Anderson and Peck 1985; Scott 1998). However, the availability of small vertebrate carcasses in nature appears limiting and is unpredictable across some levels of time and space (Wilson et al.

1984; Beninger and Peck 1992; Trumbo and Bloch 2002). As a result, co-occurring species of burying beetles face intense competition for suitable carcasses, both within and between species, and with other scavengers (Milne and Milne 1944; Wilson et al. 1984; Otronen 1988; Trumbo

1990). To avoid the costs of coexistence, co-occurring Nicrophorus species may have evolved to partition resources along spatial and temporal gradients (Anderson 1982; Wilson et al. 1984;

Beninger and Peck 1992). Specifically, evidence suggests that many Nicrophorus species have evolved to occupy different habitats. Therefore, investigations into how co-occurring

Nicrophorus species use habitats differently could further our understanding of the role habitat partitioning plays in facilitating coexistence among closely related species and provide an opportunity to examine potential underlying mechanisms of habitat partitioning.

Previous studies have described the broad habitat associations of Nicrophorus species throughout their distributions. N. orbicollis has primarily been found in forest habitats; however, they have also been captured in open fields, forest edges, and wetlands (Anderson 1982; Shubeck

1983; Anderson and Peck 1985; Lingafelter 1995; Lomolino et al. 1995; Ratcliffe 1996; Scott 11

1998; Trumbo and Bloch 2000). Similarly, N. sayi have predominantly been found in forest habitats, especially in coniferous forest, but they have also been captured in open fields at lower abundances (Anderson 1982; Anderson and Peck 1985). In contrast, N. tomentosus exhibit a broad pattern of habitat-use and have been found to be abundant in all habitat types (Anderson

1982; Shubeck 1983; Anderson and Peck 1985; Lingafelter 1995; Lomolino et al. 1995; Ratcliffe

1996; Scott 1998; Trumbo and Bloch 2000). Historically, N. pustulatus have been an enigmatic species, captured only very rarely in forest habitats and occasionally open fields (Anderson 1982;

Shubeck 1983; Anderson and Peck 1985; Robertson 1992; Lingafelter 1995; Ratcliffe 1996;

Scott 1998). However, compelling evidence suggests that the apparent rarity of N. pustulatus may be due to them being specialized to occupy the forest canopy (Ulyshen et al. 2007; LeGros and Beresford 2010; Lowe and Lauff 2012; Dyer and Price 2013; Wettlaufer et al. 2018). N. defodiens have been found only in forest habitats, with some evidence indicating that they may prefer dry coniferous forest (Anderson 1982; Anderson and Peck 1985; Trumbo and Bloch

2000). Meanwhile, N. hebes have been found almost exclusively in wetland habitats such as

Sphagnum bogs and cattail marshes, occasionally occurring in other wetland-bordering habitats

(Anderson 1982, Anderson and Peck 1985, Beninger 1989, Beninger 1994, Beninger and Peck

1992, Sikes et al. 2016). Likewise, N. marginatus appear to be habitat specialists, only occurring in large open fields and meadows (Anderson 1982; Anderson and Peck 1985; Lingafelter 1995;

Lomolino et al. 1995; Ratcliffe 1996; Dyer and Price 2013).

Four other carrion beetle species co-occur with Nicrophorus in southeastern Ontario:

Necrophila americana, Oiceoptoma inaequale, O. noveboracense, and Necrodes surinamensis

(subfamily: Silphinae). These species also feed and reproduce on carrion; however, unlike

Nicrophorus, they do not bury carcasses, do not display complex parental care, and are not 12

limited to small carcasses for breeding (Anderson and Peck 1985). The general habitat associations of these species have also been previously examined. N. americana have been found in forests, open fields, and wetlands, but are often most abundant in forest or wetland habitats

(Anderson 1982; Shubeck 1983; Anderson and Peck 1985; Lingafelter 1995; Ratcliffe 1996). O. inaequale and O. noveboracense have primarily been found in forest habitats, with O. inaequale most common in deciduous forest (Anderson 1982; Shubeck 1983; Anderson and Peck 1985;

Lingafelter 1995). In addition, both species have also been captured less commonly in open areas and marshes (Anderson 1982). Necrodes surinamensis are relatively rare compared to the other carrion beetle species and have typically only been captured in small numbers. They have been found primarily in forest and open field habitats, but have also been captured in wetlands

(Ratcliffe 1972; Anderson 1982; Lingafelter 1995; Dyer and Price 2013).

Scope of this Thesis

Here, we take the first steps towards understanding the role of habitat partitioning in facilitating the coexistence of Nicrophorus species by testing the hypothesis that co-occurring

Nicrophorus species in southeastern Ontario partition resources by associating with different habitat characteristics or distinct habitat types, potentially to facilitate coexistence. If this hypothesis is true, then we predicted that co-occurring species should be associated with different habitat characteristics within our focal study site (~3,000-hectare reserve). We tested our hypothesis by conducting intensive field surveys of carrion beetle abundance and quantitative habitat characteristics to identify and compare fine-scale differences in habitat associations across Nicrophorus species. Our study improves upon previous work by examining the associations between Nicrophorus species and 54 local habitat characteristics related to 13

substrate and vegetative properties within an environmentally diverse and heterogenous region of southeastern Ontario, where seven Nicrophorus species and four additional carrion beetle species co-occur. We performed our surveys at random sites encompassing a broad range of potential habitats to accurately reflect the available environmental diversity across the landscape. In addition, we sampled the same sites repeatedly over a four-month period to capture species as they became active throughout the season.

Chapter 2: Methods

Site Description:

We surveyed carrion beetle abundance and measured local habitat characteristics at 100 sites, randomized in their locations (with constraints, detailed below), and spanning the properties of the Queen’s University Biological Station (QUBS), near Elgin, Ontario, Canada

(Fig. 1A & 1B). These sites have been previously used for a variety of long-term studies and were originally selected by randomly generating GPS coordinates that fell within the QUBS property boundaries. We restricted initial random coordinates by two criteria: 1) sites needed to be at least 400m apart, and 2) sites could not fall in open water. The resultant sites span an area over 2690 hectares in size encompassing a broad variety of habitats including deciduous and mixed hardwood forests, conifer plantations, pine-studded rock outcrops, white cedar bogs, cattail marshes, swamps, small lakes and beaver ponds, and reclaimed agricultural fields.

Survey of Carrion Beetle Abundance:

We surveyed carrion beetle abundance between April and October 2017 using lethal pitfall traps set for seven days at a time (Wettlaufer et al. 2018). At each site, we simultaneously set one ground-level trap and a second canopy-level trap hung 6m above from a nearby tree branch. Our traps consisted of yellow plastic buckets 35cm deep and 17cm wide filled with approximately six inches of saturated saline water and baited with frozen chicken wings wrapped in cheesecloth. We suspended the chicken wings above the saline solution by wrapping a piece of steel craft wire around the chicken and attaching it to the center of a 35cm2 square of chicken wire placed over the opening of the bucket. To prevent rainfall from entering the bucket, we 15

covered each trap with a 30cm2 plywood board elevated slightly above the bucket’s lip. We then placed large stones on top of the board to deter vertebrate scavengers from disturbing the traps.

We set traps at each site three to four times over the course of the sampling period and collected all carrion beetles belonging to the family Silphidae. We then identified all carrion beetles to species and sexed them following Anderson and Peck (1985).

1 km 500 m

Fig 1. (A) Map of the 100 randomly generated sampling sites where we conducted our surveys of carrion beetle abundance and local habitat characteristics on the main properties of the Queen’s University Biological Station (QUBS). All sites are at least 400m apart and do not fall within bodies of water. (B) Sampling sites located on the Bracken tract properties of QUBS. Sites are color-coded based on the six general habitat categories assigned during our survey of habitat. The boundaries of the QUBS properties are marked by orange border lines. Base map from Google Maps (Google 2019).

Survey of Local Habitat Characteristics:

To examine the habitat associations of the collected carrion beetle species, we conducted surveys of local habitat characteristics at each of our 100 sites following a modified version of the Breeding Biology Research and Monitoring Database (BBird) field protocol for measuring vegetation (Martin et al. 1997). While originally designed for describing bird nesting sites, the

BBird protocols provide comprehensive standardized methods for measuring quantitative ground cover and vegetation characteristics that may also be relevant to burying beetles.

Ground Cover, Leaf Litter, and Soil Characteristics:

To examine the properties of the ground cover, leaf litter, and soil, we established a circular 2.5m radius plot centred on the ground-level trap at each site. We measured 2.5m from the ground-level trap in the four cardinal directions and marked these points with trail flagging tape to signify the edges of the plot. From outside of the plot, we categorized ground cover into thirteen categories and estimated the relative percentage of plot area covered by each (Table S1).

To measure leaf litter depth, we dug a small 20cm deep hole and used a ruler to measure from the top of the surface leaf litter to the soil depth at which large leaf particulate was no longer observed in the soil. We measured soil depth by pushing a 1.5m metal rod into the soil until unyielding resistance was met and measuring the length that the pole had extended below ground. We measured soil depth at four different locations in each quadrant of the plot and once at the center. We then averaged the five measures to calculate average soil depth for the site and noted the dominant soil (i.e. most common) type observed.

Habitat Type, Tree Species Diversity, and Tree Size:

To examine the number and types of trees at each site, we established a circular 17.25m radius plot centred on each ground-level trap. We measured 17.25m from the ground-level trap in the four cardinal directions and marked these spots as the edges of the plot with trail flagging tape. Within this plot, we measured the diameter at breast height (DBH) and identified to species every tree with a DBH greater than 9cm. We then categorized the forest canopy as open or closed based on whether there was dense tree cover above the site. We also placed each site into one of six general habitat categories based on the dominant vegetation and substrate type (Table

S1). Finally, using the data on tree species abundance and size, we generated an additional five variables for each site: the total number of tree species identified, the total number of trees counted, and the number of small (9 to 23cm DBH), medium (23 to 38cm DBH), and large

(>38cm DBH) trees counted within the plot.

Statistical Analyses:

In total, we caught 13,153 carrion beetles in 604 successful trapping events with all seven

Nicrophorus and four Silphinae species represented (Table 1). Prior to analyses, we removed any traps that were disturbed by vertebrate scavengers from the dataset. For our statistical analyses, we calculated the mean abundance of each carrion beetle species in the ground and canopy traps for each site over the entire trapping period. We used these values as our measure of carrion beetle abundance at each site, with ground and canopy traps handled separately.

Table 1. Counts of carrion beetles collected in ground- and canopy-level traps between April and October 2017 during our survey of carrion beetle species abundance on the properties of the Queen’s University Biological Station.

Ground-Level Canopy-Level Total Nicrophorinae Number of Number Number of Number Number of Number Species Individuals of Traps Individuals of Traps Individuals of Traps N. orbicollis 3565 180 875 127 4440 307 N. sayi 629 138 268 95 897 233 N. tomentosus 1714 99 1905 109 3619 208 N. pustulatus 37 16 491 102 528 118 N. defodiens 10 8 4 4 14 12 N. hebes 83 21 22 17 105 38 N. marginatus 3 1 0 0 3 1 Silphinae Species N. americana 2824 161 156 44 2980 205 O. inaequale 390 79 12 4 402 83 O. noveboracense 119 50 12 11 131 61 N. surinamensis 17 11 17 5 34 16 Total 9391 277 3762 327 13153 604

Conditional Inference Tree Classification:

All statistical analyses were performed in R version 3.5.1 (R Core Team 2018). To examine the associations between the mean abundances of carrion beetle species in traps, averaged across all trapping events at each site, and the local habitat characteristics surveyed, we generated conditional inference trees using the function “ctree” from the R-package “partykit” version 1.2-2 (Zeileis and Hothorn 2012). Conditional inference trees are a form of decision tree that use regression model estimates and binary recursive partitioning to group and classify data using a set of predictor variables (Hothorn et al. 2006). First, ctree estimates a regression relationship between the response variable and each predictor variable using binary recursive partitioning within a conditional inference framework. At each node of the tree, the null 19

hypothesis of independence between each predictor variable and the response variable is tested individually, and a significance value (p) assigned. The predictor variable with the lowest significance value is then used to split the data, provided that value falls below a threshold of

0.05. Splitting continues at each node down the tree until no predictor variables are found to be significantly associated with the response variable, at which point splitting stops. In our conditional inference trees, mean abundance of each species in ground and canopy traps at each site was used as the response variable while trap type (ground or canopy) and all 54 measured habitat characteristics were used as the predictor variables. Including all 55 variables allowed us to identify and describe the relationships between the habitat characteristics that most strongly influenced the abundance of each carrion beetle species within each trap. Additionally, we repeated our conditional inference tree analyses for each carrion beetle species using occurrence instead of mean abundance as the response variable. We converted our abundance data into occurrence data by recoding all mean abundances greater than zero as “present” and all zero values as “absent”. This allowed us to identify the habitat characteristics that best predicted whether a species was present or absent within a trap.

Chapter 3: Results

Habitat Associations of Carrion Beetle Species:

Our conditional inference tree analyses identified significant associations between the local habitat characteristics that we measured and the abundances and occurrence (presence versus absence) of eight carrion beetle species. N. orbicollis abundance was greater in ground- level traps (n = 100 traps; Fig 2A) and N. orbicollis were present in more traps at sites with many trees (n = 188 traps; Fig. 2B). N. sayi abundance was also greater in ground-level traps. However within ground-level traps, N. sayi abundance was higher at sites with deeper leaf litter (n = 16 traps) and a greater number of red oak (n = 13 traps), sugar maple (n = 18 traps), white pine (n =

7 traps), and small trees (n = 14 traps; Fig. 3A). N. sayi were present in a greater number of traps at sites with high numbers of trees (n = 188 traps; Fig. 3B). N. tomentosus exhibited no significant associations with any of the habitat characteristics that we measured. They were abundant (n = 199 traps; Fig. 2C) and present (n = 199 traps, Fig. 2D) in most traps that we surveyed. Both N. pustulatus abundance (n = 100 traps; Fig. 4A) and presence (n = 100 traps;

Fig. 4B) were greater in forest canopy-level traps. In contrast, no significant associations were found between N. defodiens abundance or occurrence and the habitat characteristics that we measured. N. defodiens was found in low abundance when they were captured and were absent from most traps (n = 199 traps; Fig. 5A & 5B). N. hebes abundance was greater in traps located within wetlands (n = 9 traps; Fig. 4C). However, N. hebes presence was not associated with any specific habitat characteristics. Instead, N. hebes were found to be absent from most traps (n =

199 traps; Fig. 4D). Both N. marginatus abundance (n = 8 traps; Fig. 4E) and presence (n = 8 traps; Fig. 4F) were greater in traps located within open fields. Necrophila americana abundance

(n = 100 traps; Fig. 6A) and presence (n = 100 traps; Fig. 6B) were greater in ground-level traps. 21

O. inaequale abundance was greater in ground-level traps (n = 100 traps; Fig. 6C). O. inaequale were most often present in ground-level traps, (n = 100 traps) but were also present in some canopy-level traps at sites with many red oak trees (n = 15 traps; Fig. 6D). O. noveboracense abundance (n = 100 traps; Fig. 6E) and occurrence (n = 100 traps; Fig. 6F) were greater in ground-level traps. Lastly, Necrodes surinamensis abundance and occurrence was not associated with any habitat characteristics. They were found in low abundance overall and were absent from most traps (n = 199 traps; Fig. 5C & 5D).

A) N. orbicollis - Abundance B) N. orbicollis - Presence vs. absence

C) N. tomentosus - Abundance D) N. tomentosus - Presence vs. Absence

Fig 2. Conditional inference trees showing significant associations between local habitat characteristics and (A) N. orbicollis mean abundance, (B) N. orbicollis occurrence, (C) N. tomentosus mean abundance, and (D) N. tomentosus occurrence. Boxplots show the medians, ranges, and upper and lower quartiles of mean abundance in the final groupings produced after splitting. n-values indicate the number of traps (ground and canopy) included in each node. N. 22

orbicollis abundance was greater in ground-level traps and they were present (dark shading) in a greater number of traps at sites with many trees. Neither N. tomentosus abundance nor occurrence were not significantly associated with any local habitat characteristic.

A) N. sayi - Abundance

B) N. sayi – Presence vs. Absence

Fig 3. Conditional inference trees displaying significant associations between (A) Nicrophorus sayi mean abundance and (B) N. sayi occurrence and local habitat characteristics. Boxplots show the medians, ranges, and upper and lower quartiles of mean abundance in the final groupings produced after splitting. n-values indicate the number of traps (ground and canopy) included in each node. N. sayi abundance was greater in ground-level traps at sites with deep leaf litter and 23

many red oak, sugar maple, white pine, and small trees. N. sayi were present (dark shading) in a greater number of traps at sites with many trees.

A) N. pustulatus - Abundance B) N. pustulatus - Presence vs. Absence

C) N. hebes - Abundance D) N. hebes - Presence vs. Absence

other habitats wetlands

E) N. marginatus - Abundance F) N. marginatus - Presence vs. Absence

other habitats open field other habitats open field

Fig 4. Conditional inference trees displaying significant associations between local habitat characteristics and (A) N. pustulatus mean abundance, (B) N. pustulatus occurrence, (C) N. hebes mean abundance, (D) N. hebes occurrence, (E) N. marginatus mean abundance, and (F) N. 24

marginatus occurrence. Boxplots show the medians, ranges, and upper and lower quartiles of mean abundance in the final groupings produced after splitting. n-values indicate the number of traps (ground and canopy) included in each node. Both N. pustulatus abundance and presence (dark shading) were significantly greater in canopy-level traps. N. hebes abundance was greater in traps located in wetland habitats, while N. hebes occurrence was not significantly associated with any habitat characteristics. N. marginatus abundance and presence (dark shading) were greater in traps located in open field habitat.

A) N. defodiens - Abundance B) N. defodiens - Presence vs. Absence

C) Necrodes surinamensis - Abundance D) Necrodes surinamensis - Presence vs. Absence

Fig 5. Conditional inference trees displaying significant associations between local habitat characteristics and (A) N. defodiens mean abundance, (B) N. defodiens occurrence, (C) Necrodes surinamensis mean abundance, and (D) Necrodes surinamensis occurrence. Boxplots show the medians, ranges, and upper and lower quartiles of mean abundance in the final groupings produced after splitting. n-values indicate the number of traps (ground and canopy) included in each node. No significant associations were identified between any habitat variables and the mean abundance or occurrences of either species.

A) Necrophila americana - Abundance B) Necrophila americana - Presence vs. Absence

C) Oiceoptoma inaequale - Abundance D) Oiceoptoma inaequale – Presence vs. Absence

E) Oiceoptoma noveboracense - Abundance F) Oiceoptoma noveboracense – Presence vs. Absence

Fig 6. Conditional inference trees displaying significant associations between local habitat characteristics and the abundances and occurrence of three Silphinae species. Boxplots show the medians, ranges, and upper and lower quartiles of mean abundance in the final groupings produced after splitting. n-values indicate the number of traps (ground and canopy) included in each node. (A) Necrophila americana mean abundance and (B) occurrence were greater in ground-level traps. (C) Oiceoptoma inaequale mean abundance was greater in ground-level traps. (D) O. inaequale were present (dark-shading) in a greater number of ground-level traps, 26

but they were also present in some traps at canopy-level at sites with many red oaks. (E) O. noveboracense mean abundance and (F) occurrence were greater in ground-level traps. 27

Chapter 4: Discussion

Co-occurring species of carrion beetles may partition resources to avoid interspecific competition and achieve stable coexistence. Here, we tested the hypothesis that co-occurring

Nicrophorus species in southeastern Ontario partition resources by associating with different habitat characteristics or distinct habitat types, thus potentially facilitating coexistence. We predicted that if co-occurring species partition habitat, then they should be associated with different habitat characteristics within our focal study site. Using survey data on carrion beetle abundance, occurrence, and quantitative local habitat characteristics collected from sampling sites across a environmentally diverse study site in southeastern Ontario, we successfully identified the habitat associations of six carrion beetle species in the subfamily Nicrophorinae

(Nicrophorus) and three species in the subfamily Silphinae (Necrophila, Oiceoptoma, Necrodes).

Co-occurring Nicrophorus species were found to differ in habitat use in a pattern consistent with habitat partitioning, supporting our hypothesis. The patterns of habitat-use revealed in this study suggest that the carrion beetle assemblage in southeastern Ontario consists of a mixture of habitat generalists, capable of living in a variety of conditions, and specialists that restrict their activity to specific habitats (Fig. 7).

Habitat Associations of Nicrophorinae

Our conditional inference trees predicting N. orbicollis abundance and occurrence showed that the species occupies a range of different environments, but occurs, and is most abundant in, dense forest habitats. N. orbicollis were abundant in most ground-level traps and occurred at more sites with many trees (Fig. 2A & 2B). These results suggest that N. orbicollis 28

Fig 7. The habitat associations of six co-occuring Nicrophorus species in southeastern Ontario. From left to right, habitats depicted are forest canopy, forest, wetland, and open field. Species are color-coded to represent the breadth of their habitat use; blue indicates a habitat generalist species, yellow indicates a forest generalist species, and green indicates a habitat specialist species. A trimmed molecular phylogeny is provided in the lower right corner with breadth of habitat use also indicated by color. This phylogeny was reproduced using published data from Dobler and Müller (2000), Ikeda et al. (2012), and Sikes and Venables (2013). The habitat associations of Nicrophorus defodiens are not depicted because too few were captured in our survey to identify significant associations. However, previous research has found N. defodiens to be associated with dry coniferous forest (Anderson 1982; Anderson and Peck 1985).

occur in almost all the environments we sampled, regardless of local habitat characteristics, but are less abundant in the forest canopy and are more likely to occupy forested areas. Forests may represent high quality habitat for N. orbicollis. Soils in temperate forests, such as those found at our study site in southeastern Ontario, may possess properties that make them ideal for carcass burial. In choice experiments, N. orbicollis prefer to bury carrion in soils with high organic content, such as leaf litter, as it can provide increased structural support to their brooding chambers (Muths 1991). Likewise, N. orbicollis may prefer very moist alluvial and sandy loam 29

soils, soil types that are common in temperate forests (Bishop et al. 2002; Willemssens 2015).

The temperature in forests may also provide an ideal range for N. orbicollis. Temperature can play an important role in influencing burial times (Scott 1990), the outcome of competition

(Wilson et al. 1984; Merrick and Smith 2004), rates of larval development (Smith and Heese

1995; Meierhofer et al. 1999; Nisimura et al. 2002), and activities such as flight among

Nicrophorus species (Merrick and Smith 2004). Forest canopy can have a moderating effect on below-canopy air temperature and humidity, causing maximum temperatures to be lower, and minimum temperatures and air humidity to be higher, as well as blocking UV radiation

(Grimmond et al. 2000; Renaud et al. 2011; Von Arx et al. 2012). The temperature and humidity effects are particularly important at night when N. orbicollis are active since forest canopy can buffer nocturnal heat and air moisture loss to maintain higher air temperatures and relative humidities (Renaud et al. 2011; Von Arx et al. 2012). Large beetles like N. orbicollis are prone to over-heating during intense activities such as flight, but can also struggle to produce enough energy for activity at cooler temperatures (Merrick and Smith 2004). The buffering effect of forest canopy may prevent temperatures from rising to lethal limits for N. orbicollis while keeping temperatures above the minimum required for activity. Therefore, N. orbicollis may be able to be active on a greater number of nights within forests compared to in other habitats.

N. sayi appear to be primarily associated with dense forest habitats at ground-level.

Specifically, N. sayi were more abundant at sites with deep leaf litter and many red oaks, sugar maples, white pine, and other small trees, and were present at sites with many trees (Fig. 3A &

3B). Despite occupying similar forest habitat as other Nicrophorus species, N. sayi emerge earlier in the spring and experience different environmental conditions as a result (Anderson

1982; Anderson and Peck 1985; Wettlaufer 2019). Spring conditions in temperate regions like 30

southeastern Ontario are typically colder and wetter than at other times of the year, and small vertebrates are rarer due to winter mortality (Environment Canada Climate Normals 1981 to

2010; Pucek et al. 1993). Often open habitats and those with shallow soil-layers become flooded with snow-melt and rain, likely becoming unusable to burying beetles active at the time

(Cavallaro et al. 2017). Forests with deep leaf litter layers may provide one of the few places where soils remain suitable for carcass burial and deep leaf litter may allow beetles to dig structurally stable burrows that more effectively insulate the brooding chamber (Muths 1991;

Parajulee et al. 1997; Trumbo and Bloch 2002). In addition, the tree species that N. sayi are associated with produce seeds consumed by many small vertebrates. These types of trees provide a vital source of food and refuge for overwintering and emerging small mammals; therefore, these animals tend to concentrate their activity around them (Miller and Getz 1977; Dueser and

Shugart 1978; Pyare et al. 1993; Schnurr et al. 2004). The areas around these trees may act as hotspots of small vertebrate activity and increased small vertebrate carrion availability, which could explain why N. sayi are found in greater abundance nearby.

N. tomentosus have the broadest pattern of habitat use among the Nicrophorus species of southeastern Ontario. They occurred abundantly across all environments and both abundance and occurrence were not associated with any specific habitat characteristics (Fig. 2C & 2D). These patterns suggest that N. tomentosus are habitat generalists, possessing broad environmental tolerances that allow them to survive and reproduce in a wide variety of habitats with vastly different conditions (McPeek 1996; Bonier et al. 2007). Despite overlapping in habitat-use with congeners, N. tomentosus can occupy the same habitats and avoid competition by becoming reproductively active after the reproductive season of many of the other carrion beetle species has ended (Anderson 1982; Wilson et al. 1984; Wettlaufer 2019). N. tomentosus begin emerging 31

in early August and remain active until late October (Anderson 1982; Anderson and Peck 1985;

Wettlaufer 2019). During this time period, environmental conditions in southeastern Ontario undergo rapid and dramatic changes in temperature, rainfall, and day-length (Environment

Canada Climate Normals 1981 to 2010). As such, N. tomentosus could require broad environmental tolerances to cope with the changing climatic conditions. Part of this tolerance may be facilitated through behavioural traits. N. tomentosus are active diurnally and submerge carcasses in shallow pits under groundcover rather than fully burying them (Shubeck 1971;

Anderson and Peck 1985). By shifting their activity to earlier in the day and reducing the time required to prepare carrion by burying carcasses in shallow pits, N. tomentosus may be able to find and secure carcasses quickly while temperatures are higher during the day. Furthermore, burying carrion in shallow pits under groundcover may reduce the influence of local soil properties on brood chamber structure and larval development, while also aiding in reducing flood risk. In addition, the larvae of N. tomentosus may be particularly tolerant of challenging conditions, as the species uniquely overwinters in the larval stage and face the environmental extremes of winter as larvae (Anderson 1982). N. tomentosus may possess traits that confer broad tolerance to seasonally changing environmental conditions and this may also allow them to take advantage of many different habitats.

N. pustulatus have historically been regarded as an enigmatic species rarely captured in field surveys and little is known of their natural history (Anderson 1982; Shubeck 1983;

Anderson and Peck 1985; Robertson 1992; Lingafelter 1995; Ratcliffe 1996; Scott 1998). Recent evidence suggests that their apparent rarity may be due to them being forest canopy specialists and therefore less likely to be captured in the ground-level pitfall traps typically employed

(Ulyshen et al. 2007; LeGros and Beresford 2010; Lowe and Lauff 2012; Dyer and Price 2013; 32

Wettlaufer et al. 2018). Our results provide further evidence supporting the idea that N. pustulatus are forest canopy specialists. In our analyses, high N. pustulatus abundance and occurrence were best predicted by forest-canopy level traps (Fig. 4A & 4B); no other habitat variables predicted N. pustulatus occurrence or abundance. By diverging into the forest canopy,

N. pustulatus may be able to escape competition with co-occurring congeners and take advantage of novel canopy resources (Ulyshen et al. 2007; Wettlaufer et al. 2018). Other carrion beetle species are largely absent from the forest canopy or occur in substantially lower abundances

(Ulyshen et al. 2007; Dyer and Price 2013; Wettlaufer et al. 2018). These species may be unable to meet the energetic demands and lack the maneuverability required to maintain flight to search for carrion in the forest canopy (Berwaerts et al. 2002; Merrick and Smith 2004; Wettlaufer et al.

2018). Meanwhile, many small vertebrates like birds use tree cavities and branches located in the upper forest canopy as nesting sites during their breeding season, providing a reliable source of carrion for N. pustulatus (Ricklefs 1969). N. pustulatus are also capable of reproducing on larger carcasses (>100g) and can produce significantly more offspring than congeners, which could allow them to maximize reproductive output when opportunities present themselves if carrion is rare in the canopy (Robertson 1992; Trumbo 1992). However, how N. pustulatus bury carrion in the forest canopy is currently not well understood. N. pustulatus have been demonstrated to bury carcasses like other Nicrophorus species when provided suitable substrate in laboratory experiments (Robertson 1992), and have been observed to bury nestling bird carcasses in nest lining within a nest box of Tree Swallows (Tachycineta bicolor; Wettlaufer et al. 2018). To date,

N. pustulatus reproduction in the forest canopy has not been observed in nature and the natural history of the species remains enigmatic. 33

Neither N. defodiens abundance nor occurrence were associated with any of the habitat characteristics we surveyed. N. defodiens were predicted to be either rare or absent in most traps, regardless of the surrounding environment, suggesting that this species is rare at our study site

(Fig. 5A & 5B). In total, only 14 individuals were captured at 10 different sites over our entire sampling period (Table 1). Previous studies have reported strong associations between N. defodiens and forested habitats and indicate they may prefer dry coniferous forest (Anderson

1982; Anderson and Peck 1985; Trumbo and Bloch 2000). Our analyses may have been unable to identify any significant associations between N. defodiens and local habitat characteristics due to the low number of N. defodiens captured in our survey, and the rarity of coniferous forest at our study site (only two of our trapping sites were located within coniferous forest; Fig. 1A).

Alternatively, N. defodiens could be generally rare in southeastern Ontario. Other surveys of carrion beetle abundance in southeastern Ontario performed by Anderson (1982) and Robertson

(1992) also found N. defodiens to be uncommon in the region.

The habitat associations of N. hebes indicate that they are wetland specialists, as has previously been suggested (Anderson 1982; Beninger and Peck 1992; Sikes et al. 2016). Our analysis found that N. hebes abundance was greater in wetland habitats than in all other habitat types combined. N. hebes occurrence was not associated with any habitat characteristics (Fig. 4C

& 4D), likely reflecting our ability to trap N. hebes in small numbers in other habitats, provided that wetlands are nearby. The presence of open water, water-saturated and oxygen-limited soils and acidic or basic pH-levels common in wetlands likely pose substantial challenges for burying beetles (Batzer and Wissinger 1996), leading to the question of how N. hebes is able to breed in wetland habitat. In captivity, N. hebes have been demonstrated to bury carcasses and rear broods like other Nicrophorus species when provided suitable soil, suggesting they do not exhibit an 34

alternative reproductive strategy (Beninger 1989). N. hebes instead likely possess unique adaptations that aid in survival and reproduction in wetland environments, and they may restrict their activity to areas within wetlands that facilitate carcass burial. Burying beetles have been shown to tolerate immersion under water and hypoxic conditions better than non-burying carrion beetles, but performance differs between Nicrophorus species, and N. hebes has not been specifically tested (Cavallaro et al. 2017). In any case, adult N. hebes can likely escape submersion by avoiding pools of open water and retreating above ground when water levels rise.

Burial chambers in wetlands, however, likely become inundated with water frequently, and thus

N. hebes larvae may require adaptations to frequent immersion and hypoxia. For example, the larvae of marsh-dwelling tiger beetles (spp. Cicindela togata) can survive up to 6 days submerged underwater by severely reducing metabolic activity via dormancy and using anaerobic metabolic pathways (Hoback et al. 1998; Hoback and Stanley 2001). Alternatively, some terrestrial insects frequently exposed to submersion can trap small air bubbles on their bodies to serve as a physical gill or absorb oxygen from water directly through their cuticle

(Foster and Treherne 1976; Hoback and Stanley 2001; Pedersen and Colmer 2012). In addition, flooding in Nicrophorus burial chambers can result in the release of volatile organic compounds from buried carcasses and the presence of these compounds can interfere with the beetle’s metabolic pathways and reduce the time beetles can survive immersed (Cavallaro et al. 2017). In response, N. hebes may bury carcasses close to the surface in shallow pits like their sister species

N. vespilloides or, when possible, hide carcasses under groundcover to prevent complete restriction of airflow (Pukowski 1933; Anderson and Peck 1985). Furthermore, to limit the risk of submersion, N. hebes may limit their activity to areas within wetlands with drier substrate 35

such as sphagnum moss, shorelines, and raised islands (Beninger 1989, 1994; Beninger and Peck

1992).

N. marginatus were also identified as habitat specialists and were significantly more likely to occur, and be abundant, in open fields than in other habitats (Fig. 4E & 4F). These findings are consistent with the conclusions of most existing literature on N. marginatus habitat associations (Anderson 1982; Anderson and Peck 1985; Lingafselter 1995; Lomolino et al. 1995;

Ratcliffe 1996; Dyer and Price 2013). However, very few N. marginatus were captured in our survey. Over the entire survey, only 3 individuals were collected from a single trap (Table 1).

This contrasts with other parts of their range where N. marginatus are among the most abundant

Nicrophorus species (Lingafelter 1995; Backlund and Marrone 1997). N. marginatus has been suggested to prefer very large open fields and meadows greater than 25 hectares in size (Trumbo and Bloch 2000). This preference may have limited our ability to capture the species, as large fields are uncommon in our study area and we successfully trapped N. marginatus at only one open field site. Regardless, open fields likely present considerable challenges for Nicrophorus species. Lacking any forest canopy, open fields are exposed to high levels of sunlight and rainfall. As a result, the ambient air and soil conditions in open fields during the summer are often hotter, drier, and prone to temporary flooding (Renaud et al. 2011; Von Arx et al. 2012).

Interestingly, N. marginatus have been found to exhibit relatively high rates of water loss in dry, low humidity conditions, contrary to what would be expected based on their habitat associations

(Bedick et al. 2006). To avoid desiccation and lethal temperatures, they may respond to dry conditions by limiting their activity to times of the day when temperatures are cooler and spending their time burrowed in moist soils within fields (Bedick et al. 2006). Currently, little is 36

known of what other adaptations N. marginatus may possess for circumventing the challenges presented by open field conditions.

Habitat Associations of Silphinae

The four Silphinae carrion beetle species included in our analyses were all found to display generalist habitat preferences consistent with existing literature (Ratcliffe 1972, 1996;

Anderson 1982; Shubeck 1983; Anderson and Peck 1985; Lingafelter 1995; Dyer and Price

2013). Necrophila americana were found to be abundant and present in ground-level traps in all habitat types (Fig. 6A & 6B). Since N. americana feed and reproduce on carrion of all sizes and do not display complex parental care, having broad habitat associations likely allows them to take advantage of more carcasses wherever they appear (Anderson and Peck 1985). Furthermore,

N. americana are the most abundant Silphinae species in southeastern Ontario and are significantly larger than the other common Silphinae species (Oiceoptoma inaequale and O. noveboracense; Table 1; Anderson and Peck 1985; Ratcliffe 1996; Collard 2018). As such, N. americana likely do not face significant competitive pressures from Nicrophorus, which are limited to small carcasses, nor from other Silphinae, leaving them unrestricted to occupy all available habitats. O. inaequale and O. noveboracense also display generalist habitat associations, although previous studies suggest that O. inaequale is more abundant in deciduous forest (Anderson 1982; Shubeck 1983; Anderson and Peck 1985; Lingafelter 1995). Both species were most abundant and occurred most often in ground-level traps, but O. inaequale also occurred in lower abundance in some canopy-level traps at sites with many red oak trees (Fig.

6C-F). O. inaequale and O. noveboracense may emerge early in spring to avoid competition with larger carrion beetles such as N. americana (Anderson 1982; Anderson and Peck 1985). The 37

tendency for O. inaequale to occupy deciduous forest with many red oaks likely reflects similar reasons as those discussed for N. sayi; small vertebrates emerging from winter hibernacula likely congregate near seed-bearing trees like oaks and maples creating concentrated areas of available carrion. It’s unclear why O. noveboracense does not display similar associations, however, it may be that at our study site O. inaequale is able to outcompete O. noveboracense for higher quality forest habitat. In many areas of their distributions; one species is usually rare or absent

(Anderson and Peck 1985; Ratcliffe 1996). In our survey, both species were collected and often in the same trap. Yet, over the entire trapping period, we caught four times as many O. inaequale as O. noveboracense suggesting that O. inaequale are at least numerically dominant at our study site (Table 1). Lastly, Necrodes surinamensis were rare in our survey and no significant habitat associations were identified with their abundance or occurrence (Fig. 5C & 5D). In nature,

Necrodes surinamensis seek out large carrion such as deer for reproduction and the adults feed primarily on fly maggots (Ratcliffe 1972; Anderson 1982; Anderson and Peck 1985). Thus, the chicken wings we used to bait our traps may have been insufficient to attract them in large numbers or they may be rare in the area, as has previously been found (Anderson 1982).

General Patterns of Habitat Use

The patterns of habitat differences identified among some Nicrophorus in southeastern

Ontario – in particular, the three habitat specialists (N. pustulatus, N. hebes, N. marginatus) - could be the result of a variety of non-mutually exclusive processes. Foremost, competition for limiting resources could influence the distribution of species across habitats (Connell 1961; Ziv et al. 1993; Wisheu 1998). Aggressive interactions among Nicrophorus species are highly asymmetric and the outcomes of such interactions are primarily mediated by body size, with 38

larger beetles typically winning contests for resources (Otronen 1988; Safryn and Scott 2000).

Large species such as N. orbicollis may be competitively dominant and competitively exclude smaller species from high-quality habitats such as forest (Hardin 1960; Anderson 1982; Trumbo

1990; Ziv et al. 1993). As a result, smaller or less competitive species like N. pustulatus, N. defodiens, N. hebes, and N. marginatus may be forced into lower quality habitats like wetlands and open fields. To avoid the costs associated with reproducing in low quality habitat, specialist species may have evolved adaptations to their local environments that aid in survival and reproduction or they may possess broader environmental tolerances (Morse 1974; Toft 1985;

McPeek 1996; Irschick et al. 1999; Hilton et al. 2008; Dreiss et al. 2012). In contrast, competitively dominant species like N. orbicollis may be able to monopolize higher quality habitats, but lack the adaptations or tolerance required to also occupy and persist in lower quality, marginal habitats. Alternatively, Nicrophorus species may be deterred from occupying the same habitats due to costs imposed by frequency-dependent increases in parasitism, predation, or disease (Freeland 1983; Martin 1988a, 1988b). Such interactions are poorly described for carrion beetles, and the overall impacts of these selective pressures on populations of carrion beetles are not well understood. Dispersal limitations could also explain patterns of habitat partitioning if species are unable to colonize novel habitats due to distance or physical barriers (MacArthur 1958; Diamond 1975). Yet, the mosaic nature of habitats at our study sites, with different habitats occurring in close proximity, and the ability of carrion beetles to move large distance (Bedick et al. 1999; Attisano and Kilner 2015), suggests that dispersal limitation is unlikely to restrict habitat use at our site. Finally, the habitat differences among carrion beetles could reflect historical factors or have arisen due to chance during a species evolutionary history, and thus not reflect contemporary selective pressures or interactions among co-occurring species 39

(Connell 1980; Vellend 2010). To identify the specific mechanisms underlying differences in habitat use, we require measures of relative competitive and reproductive performance and tests among these alternative hypotheses (Hairston 1980a; Wisheu 1998; Blanquart et al. 2013). This could be accomplished using reciprocal transplants and removal experiments to examine species’ performance when in different habitats and in the presence or absence of competitor species.

Three other Nicrophorus species (N. orbicollis, N. sayi, N. tomentosus) overlapped heavily in habitat use but likely partition resources along a different environmental gradient. N. orbicollis, N. sayi, and N. tomentosus are frequently found in the same habitats and may instead partition resources temporally by separating their reproductive seasons (Anderson 1982; Wilson et al. 1984; Wettlaufer 2019). N. sayi is the first Nicrophorus species to emerge in the spring and is reproductively active in our region from late April to June (Anderson 1982; Wilson et al.

1984; Anderson and Peck 1985; Wettlaufer 2019). N. orbicollis is primarily active in the summer from June to August and is typically the most abundant Nicrophorus species during this time

(Anderson 1982; Wilson et al. 1984; Anderson and Peck 1985; Wettlaufer 2019). N. tomentosus emerges later, with peak numbers from late July to early October (Anderson 1982; Wilson et al.

1984; Anderson and Peck 1985; Wettlaufer 2019). These three species may thus be able to coexist, despite relying on similar resources for reproduction, by partitioning these resources through time (seasons) instead of space (habitat).

Other species that overlap in habitat-use and seasonal activity may reduce shared resource requirements by reproducing on different sizes of carrion (Trumbo 1990, 1992; Ikeda et al. 2006). For example, N. defodiens can reproduce on significantly smaller carrion than N. orbicollis and thus avoid competition for very small carcasses (Trumbo 1990). In addition, smaller Nicrophorus species may be more efficient at exploiting available carrion resources 40

(Persson 1985; Vance 1985). Smaller species like N. tomentosus, N. defodiens, and N. hebes are diurnal and become active earlier in the day than their larger, predominantly nocturnal, competitors (Shubeck 1971; Anderson and Peck 1985; Scott 1998). Becoming active earlier may provide an advantage against competitors by allowing these species to find and secure carrion before larger species become active (Trumbo and Bloch 2002). Additionally, these species may be able to hide carcasses from competitors and other scavengers more quickly by submerging carrion into shallow pits under leaf litter rather than fully burying it (Anderson and Peck 1985;

Trumbo and Bloch 2002).

The patterns of habitat use that we found in southeastern Ontario mirror those observed in

Nicrophorus assemblages in other regions of the world. Many Nicrophorus species appear to share similar generalist habitat associations and preferences for forested areas as those exhibited by N. orbicollis and N. sayi. These include the Palearctic species N. vespilloides, N. maculifrons,

N. interruptus, N. sepultor, and N. quadripunctatus, the North American species N. guttula, and the Central American species N. mexicanus (Anderson and Peck 1985; Růžička 1994; Ratcliffe

1996; Ohkawara et al. 1998; Dekeirsschieter et al. 2011; Urbański and Baraniak 2015; Çiftçi et al. 2018). The widely distributed Holarctic species N. investigator appears to display a similar breadth of habitat use as N. tomentosus, being found in forests, open habitats, high and low elevations, and the forest canopy (Smith and Heese 1995; Ratcliffe 1996; Ohkawara et al. 1998;

Scott 1998; Trumbo and Bloch 2000; Dekeirsschieter et al. 2011; Çiftçi et al. 2018). Like N. pustulatus, both N. investigator and N. tenuipes have been found to be common in the forest canopy in Japan, suggesting that vertical partitioning may be an important axis of resource partitioning among Nicrophorus (Ohkawara et al. 1998; Wettlaufer et al. 2018). The broadly distributed Palearctic species N. humator shares a preference for coniferous forest, as has been 41

suggested for N. defodiens (Růžička 1994; Scott 1998; Urbański and Baraniak 2015; Çiftçi et al.

2018). Likewise, throughout their distribution in northern Europe and East Asia, N. vespillo are predominantly associated with open fields similar to N. marginatus (Scott 1998; Dekeirsschieter et al. 2011; Urbański and Baraniak 2015; Çiftçi et al. 2018), but have also been found to be abundant in moist marshland (Růžička 1994), like N. hebes. Open-field specialists like N. marginatus also appear to be common in other assemblages. Species such as N. antennatus, N. germanicus, and N. vestigator in Europe and Asia, and N. hybridus, N. obscurus and N. carolinus in North America are primarily found in large open fields, meadows, prairies, and steppe habitats

(Anderson and Peck 1985; Růžička 1994; Lingafelter 1995; Ratcliffe 1996; Scott 1998;

Dekeirsschieter et al. 2011; Urbański and Baraniak 2015; Çiftçi et al. 2018). Despite these apparent similarities, the habitat associations of many Nicrophorus species remain poorly known and only a limited selection of habitats have been surveyed in most regions. Future investigations of the habitat associations of Nicrophorus in regions of Europe and Asia may clarify similarities and differences in habitat use among co-occurring Nicrophorus species and identify some of the recurrent selective pressures that influence carrion beetles across communities.

In conclusion, we found that co-occurring Nicrophorus species in southeastern Ontario differ in their use of habitats in a pattern consistent with habitat partitioning. Our results show that three Nicrophorus species have specialist associations with habitats where other

Nicrophorus species are less common, while another three Nicrophorus species exhibit generalist habitat associations and overlap highly in habitat use with other co-occurring species. These

Nicrophorus species that did not differ in habitat use are those that may instead partition through reproductive timing (Wettlaufer 2019). Our findings suggest that habitat may be an important resource axis along which some Nicrophorus species partition, however, other resource axes may 42

also be important for Nicrophorus coexistence. Further investigations will be needed to determine if habitat partitioning has truly occurred in response to species interactions and to identify the underlying mechanisms responsible. Nonetheless, our findings represent a crucial first step towards understanding the role of habitat partitioning in facilitating coexistence between co-occurring Nicrophorus species and furthers our understanding of both how closely related species coexist and of the processes that ultimately shape local diversity.

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Appendix A: Supplementary Materials

Table S1. Names, abbreviations used in analyses, and descriptions of all 55 predictor variables measured in our surveys of local habitat characteristics and used in our statistical analyses. Diameter at breast height is abbreviated as DBH in all relevant descriptions.

Variable Abbreviation Description Trap type “Trap” Ground-level or canopy-level lethal pitfall trap; canopy traps were suspended 6m above the ground and were paired with a ground-level trap at each site Habitat type “Habitat” The type of habitat at each site, based on the dominant vegetation and substrate type. Six categories: deciduous forest, coniferous forest, mixed forest, rocky outcrop, wetland, and open field Dominate substrate type “Substrate” The most abundant type of substrate at a site. Five categories: loose soil, sandy soil, hard soil, muddy soil, and rock Average soil depth (cm) “Depth” The average soil depth at a site in centimetres Leaf litter depth (cm) “Litter” The depth of the leaf litter layer at a site measured in centimetres Forest canopy “Canopy” Open or closed tree canopy Percent ground covered by grass “Grass” The percentage of ground in our 2.5m radius plots covered by grass Percent ground covered by rock “Rock” The percentage of ground in our 2.5m radius plots covered by rock Percent ground covered by leaf litter “Leaf” The percentage of ground in our 2.5m radius plots covered by leaf litter Percent bare ground “Bare” The percentage of bare ground in our 2.5m radius plots Percent ground covered by sedge “Sedge” The percentage of ground in our 2.5m radius plots covered by sedge Percent ground covered by shrubs “Shrub” The percentage of ground in our 2.5m radius plots covered by shrubs Percent ground covered by saplings “Sapling” The percentage of ground in our 2.5m radius plots covered by small saplings Percent ground covered by brush “Brush” The percentage of ground in our 2.5m radius plots covered by brush Percent ground covered by ferns “Fern” The percentage of ground in our 2.5m radius plots covered by ferns Percent ground covered by moss “Moss” The percentage of ground in our 2.5m radius plots covered by mosses Percent ground covered by marsh “Marsh” The percentage of ground in our 2.5m radius plots covered by marsh vegetation vegetation Percent ground covered by open “Water” The percentage of ground in our 2.5m radius plots covered by open water water 68

Percent ground covered by fallen logs “Log” The percentage of ground in our 2.5m radius plots covered by fallen logs Number of sugar maples (Acer “Sugar.Maple” The number of sugar maples with DBH greater than 9cm counted within our 17.25m radius saccharum) plots Number of white ashes (Fraxinus “White.Ash” The number of white ashes with DBH greater than 9cm counted within our 17.25m radius americana) plots

Number of white birches (Betula “White.Birch” The number of white birches with DBH greater than 9cm counted within our 17.25m radius papyrifera) plots Number of American beeches (Fagus “American.Beech” The number of American beeches with DBH greater than 9cm counted within our 17.25m grandifolia) radius plots Number of eastern white pines (Pinus “White.Pine” The number of eastern white pines with DBH greater than 9cm counted within our 17.25m strobus) radius plots Number of red juniper (Juniperus “Red.Cedar” The number of red junipers with DBH greater than 9cm counted within our 17.25m radius virginiana) plots Number of red maples (Acer rubrum) “Red.Maple” The number of red maples with DBH greater than 9cm counted within our 17.25m radius plots Number of green ashes (Fraxinus “Green.Ash” The number of green ashes with DBH greater than 9cm counted within our 17.25m radius pennsylvanica) plots Number of basswoods (Tilia “Basswood” The number of basswoods with DBH greater than 9cm counted within our 17.25m radius americana) plots Number of red oaks (Quercus rubra) “Red.Oak” The number of red oaks with DBH greater than 9cm counted within our 17.25m radius plots Number of ironwoods (Ostrya “Ironwood” The number of ironwoods with DBH greater than 9cm counted within our 17.25m radius virginiana) plots Number of white elms (Ulmus “White.Elm” The number of white elms with DBH greater than 9cm counted within our 17.25m radius americana) plots Number of dead trees “Dead” The number of dead trees with DBH greater than 9cm counted within our 17.25m radius plots Number of red pines (Pinus resinosa) “Red.Pine” The number of red pines with DBH greater than 9cm counted within our 17.25m radius plots Number of silver maples (Acer “Silver.Maple” The number of silver maples with DBH greater than 9cm counted within our 17.25m radius saccharinum) plots Number of white oaks (Quercus “White.Oak” The number of white oaks with DBH greater than 9cm counted within our 17.25m radius alba) plots Number of trembling aspens “Trembling.Aspen” The number of trembling aspens with DBH greater than 9cm counted within our 17.25m (Populus tremuloides) radius plots Number of bigtooth aspens (Populus “Bigtooth.Aspen” The number of bigtooth aspens with DBH greater than 9cm counted within our 17.25m grandidentata) radius plots Number of blue beeches (Carpinus “Blue.Beech” The number of blue beeches with DBH greater than 9cm counted within our 17.25m radius caroliniana) plots 69

Number of eastern white cedar “Nothern.White.Cedar” The number of eastern white cedars with DBH greater than 9cm counted within our 17.25m (Thuja occidentalis) radius plots Number of eastern hemlocks (Tsuga “Eastern.Hemlock” The number of eastern hemlocks with DBH greater than 9cm counted within our 17.25m canadensis) radius plots Number of black cherry trees (Prunus “Black.Cherry” The number of black cherry trees with DBH greater than 9cm counted within our 17.25m serotina) radius plots Number of shagbark hickory trees “Shagbark.Hickory” The number of shagbark hickory trees with DBH greater than 9cm counted within our (Carya ovata) 17.25m radius plots Number of crab apple trees (genus “Crab.Apple” The number of crab apple trees with DBH greater than 9cm counted within our 17.25m Malus) radius plots Number of rock elms (Ulmus “Rock.Elm” The number of rock elms with DBH greater than 9cm counted within our 17.25m radius thomasii) plots

Number of white spruces (Picea “White.Spruce” The number of white spruces with DBH greater than 9cm counted within our 17.25m glauca) radius plots Number of black ashes (Fraxinus “Black.Ash” The number of black ashes with DBH greater than 9cm counted within our 17.25m radius nigra) plots Number of yellow birches (Betula “Yellow.Birch” The number of yellow birches with DBH greater than 9cm counted within our 17.25m alleghaniensis) radius plots Number of common buckthorns “Common.Buckthorn” The number of common buckthorns with DBH greater than 9cm counted within our (Rhamnus cathartica) 17.25m radius plots Number of pear hawthorns “Pear.Hawthorn” The number of pear hawthorns with DBH greater than 9cm counted within our 17.25m (Crataegus calpodendron) radius plots Number of slippery elms (Ulmus “Slippery.Elm” The number of slippery elms counted within our 17.25m radius plots rubra) Total number of tree species “Total.Tree.Species” The total number of tree species identified with DBH greater than 9cm within our 17.25m radius plots Total number of trees “Total.Trees” The total number of trees with DBH greater than 9cm counted within our 17.25m radius plots Total number of small trees “Small.Trees” The total number of trees with DBH between 9cm and 23cm counted within our 17.25m radius plots Total number of medium trees “Medium.Trees” The total number of trees with DBH between 23cm and 38cm counted within our 17.25m radius plots Total number of large trees “Large.Trees” The total number of trees with DBH greater than 38cm counted within our 17.25m radius plots 70