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Spring 2019
Spatio-temporal niche patterns and thermal environmental cues: Implications for the persisitence of Nicrophorine burying beetles
Maranda Lillian Keller University of New Hampshire, Durham
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Recommended Citation Keller, Maranda Lillian, "Spatio-temporal niche patterns and thermal environmental cues: Implications for the persisitence of Nicrophorine burying beetles" (2019). Master's Theses and Capstones. 1275. https://scholars.unh.edu/thesis/1275
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SPATIO-TEMPORAL NICHE PATTERNS AND THERMAL ENVIRONMENTAL CUES:
IMPLICATIONS FOR THE PERSISTENCE OF NICROPHORINE BURYING BEETLES
BY
MARANDA L. KELLER
Bachelor of Science, Oklahoma State University, 2016
THESIS
Submitted to the University of New Hampshire
in Partial Fulfillment of
the Requirements for the Degree of
Master of Science
in
Biological Sciences: Integrative and Organismal Biology
May, 2019
This thesis/dissertation has been examined and approved in partial fulfillment of the requirements for the degree of MS in Integrative and Organismal Biology by:
Thesis Director, Dr. Carrie L. Hall, Assistant Professor of Ecology and
Biology Education (Integrative Organismal Biology)
Dr. Daniel Howard, Assistant Professor (Integrative Organismal Biology)
Dr. Thomas Lee, Associate Professor
(Natural Resources and the Environment)
On 05/02/2019
Original approval signatures are on file with the University of New Hampshire Graduate School.
ii DEDICATION
This thesis is dedicated to my family. To my parents who support and love me as I pursue what I am passionate about. Thank you for your enthusiasm over the years and for setting an example of hard work and dedication. To Brianne who never fails to make me feel like I can accomplish anything and to Clarice who keeps me young. Thank you for your encouragement and for always making me feel loved.
iii ACKNOWLEDGEMENTS
I would like to thank Dr. Carrie Hall for taking me on as her graduate student and exposing me to the unique and curious ecologies of the burying beetles. I would also like to thank my thesis committee members, Dr. Daniel Howard and Dr. Tom Lee, for sharing their expertise and guiding me throughout these projects. Thank you to Sarah Dodgin, Mia Phillips and Brooke Woelber who not only helped me immensely with lab and field work, but also listened to me, laughed with me, and inspired me. Lastly, thank you to all the undergraduate research technicians in the Hall and Howard labs who were integral to the field and lab work that made these projects possible.
iv
TABLE OF CONTENTS DEDICATION ...... iii ACKNOWLEDGEMENTS ...... iv LIST OF TABLES ...... vi LIST OF FIGURES ...... vii ABSTRACT ...... viii INTRODUCTION ...... 1 The Ecological Niche ...... 1 Climate Change Impacts on Ecological Interactions ...... 4 The Burying Beetles ...... 7 Project Goals ...... 11 CHAPTER 2 – SPATIO-TEMPORAL NICHE USE PATTERNS OF SYMPATRIC NICROPHORUS SPP...... 13 Introduction ...... 13 Methods ...... 16 Results ...... 19 Discussion ...... 21 Tables ...... 24 CHAPTER 3 – THERMAL ENVIRONMENTAL CUES ON THE REPRODUCTIVE BIOLOGY OF NICROPHORUS MARGINATUS ...... 33 Introduction ...... 33 Methods ...... 36 Results ...... 40 Discussion ...... 41 Figures ...... 46 CONCLUSION ...... 53 REFERENCES ...... 57
v
LIST OF TABLES
CHAPTER 2
2.1. Core range estimates 24
2.2. Spatial overlap estimates 25
2.3. Pair-wise spatial overlap estimates 26
2.4. Temporal activity peaks 27
2.5. Pair-wise temporal overlap coefficients 28
vi LIST OF FIGURES
CHAPTER 2
2.1. Spatial segregation of N. marginatus and N. orbicollis 29
2.2. Mean interspecies core range overlap 30
2.3. Pair-wise percent core range overlap 31
2.4. Temporal activity patterns 32
CHAPTER 3
3.1. Experimental design 45
3.2. Activity monitor set-up 46
3.3. Burial duration in varying rearing temperatures 47
3.4. Burial duration due to parental rearing temperatures 48
3.5. Reproductive success rates 49
3.6. Offspring parameters 50
3.7. Movement activity 51
vii ABSTRACT
SPATIO-TEMPORAL NICHE PATTERNS AND THERMAL ENVIRONMENTAL CUES:
IMPLICATIONS FOR THE PERSISTENCE OF NICROPHORINE BURYING BEETLES
by
Maranda L. Keller
University of New Hampshire
The persistence of burying beetles (Silphidae: Nicrophorus) depends on the successful acquisition of a highly competitive resource. Breeding pairs of the Nicrophorine genus work together to bury and prepare a suitable carcass as food for their developing larvae. To understand the mechanisms allowing for the persistence of multiple burying beetle species in Nicrophorine- rich communities, this thesis explores how sympatric burying beetles utilize space and time to partition the carrion resource. Further, to explore how thermal environments influence the reproductive biology of burying beetles, the response of Nicrophorus marginatus, both within and across generations is measured by monitoring rearing behaviors, movement activity, and brood characteristics with exposure to varying temperature regimes. The results of these studies present an important interplay between space use and temporal activity patterns that may serve to mediate negative interactions among sympatric buying beetle species. Generally, where species exhibit high temporal or spatial overlap, they are segregated along the alternative niche dimension. Future work on this community of burying beetles should examine the trophic ecology of species that appear to overlap spatially and temporally. The findings of these studies also indicate that increasing temperatures may impose direct fitness consequences on populations of N. marginatus. While this species appears to exhibit higher activity in elevated temperatures, they also exhibited extended burial timing and significantly reduced reproductive success rates.
viii Efforts should be made to increase our understanding of the thermal capacity of the Nicrophorine genus as a whole.
ix INTRODUCTION
The Ecological Niche
Stable coexistence of organisms is facilitated through differences in species’ ecological niches. A species’ ecological niche is defined as all biotic interactions, abiotic conditions and resource qualities with which it can persist indefinitely (Hutchinson 1957). The realm within this range where environmental conditions are suitable for a species’ persistence is that species’ fundamental niche (Hutchinson 1957). In the absence of co-occurring species, an organism could feasibly utilize its entire fundamental niche. However, the presence of interspecific interactions further restrict the niche space occupied by a species to its realized niche (Hutchinson 1957).
Theory posits that in order for species of similar ecology to coexist, their ecological niche must differ to some degree (Gause 1932, Hardin 1960, Schoener 1974). Often, communities house a suite of coexisting organisms that appear to assume identical ecological roles. However, niche theory suggests that these seemingly redundant species are using their resources differently. By closely examining resource acquisition strategies, spatial abundances, and the temporal activity of closely related species, cryptic patterns of contrasting resource use emerge
(Hardin 1960, Pianka 1973, Schoener 1974). Such niche differences are integral in maintaining species diversity and therefore drive ecosystem functions (Loreau and Hector 2001, Hooper et al.
2005, Balvanera et al. 2006, Levine and HilleRisLambers 2009). Examples of niche partitioning along the resource, spatial, and temporal axes are abundant in the literature and offer insight into the mechanisms underlying species coexistence.
How organisms obtain essential resources plays an important role in shaping ecological communities given the importance of trophic interactions to ecosystem health (Holt and Loreau
2002). Differing resource acquisition strategies allows for contrasting essential resource
1 requirements and thus stable coexistence. For instance, variation in pitcher form and trapping features in sympatric Nepenthes pitcher plant species allow for capture of differential prey type
(Gaume et al. 2016). This trophic separation mediating coexistence has been documented for organisms of diverse taxa including termites, bees, lizards, rodents, bats, and seabirds (Grinnell
1917, Brown and Lieberman 1973, Aguiar et al. 2013, Navarro et al. 2013, Carvalho et al. 2014,
Falk et al. 2015, Li et al. 2015, Murray et al. 2016). Differences in resource use also have been documented to mediate coexistence between exotic and native organisms by reducing negative interactions. For instance, trophic separation between native and introduced salmonid fish co- occurring in a oligotrophic lake is speculated as the mechanism facilitating their long-term coexistence (Juncos et al. 2015). A similar pattern has also been documented in an exotic-native species complex of piranhas – their contrasting carbon stable isotope signatures suggest differential prey types (Alves et al. 2017).
Spatial niche partitioning, where species vary in their space use patterns, is an additional modality through which niche partitioning occurs (Chesson 2000). This form of niche partitioning facilitates the persistence of species that do not differ in their resource use, as spatial separation mediates direct competition (Amarasekare 2003). Examples of spatial segregation amongst similar species are exhibited in diverse ways. For example, spatial partitioning along the forest strata has been documented to occur for species that only exist in the canopies of tropical forests (Vieira and Monteiro-Filho 2003, Voigt 2010, Roswag et al. 2015). Further, spatial separation allows for the optimal exploitation of limited reproductive space as exhibited by multiple dung beetle species that reproduce simultaneously on a single dung pad (Chao et al.
2013); or by wood-boring beetles that segregate reproductive space on the basis of dead wood size or moisture content (Borkowski and Skrzecz 2016, Satoh et al. 2016). Examples of spatial
2 niche partitioning are abundant and span across taxa including organisms such as parasitoids, feather mites, ants, spiders, birds, lizards, small mammals, and ungulates (MacArthur 1958,
Schoener 1968, Albrecht and Gotelli 2001, Pokharel et al. 2015, Samra et al. 2015, Stefan et al.
2015, Michalko et al. 2016, Zhong et al. 2016, Estavo et al. 2017, Winchell et al. 2018).
Although less studied than resource or spatial niche partitioning, temporal niche partitioning represents an important means by which similar species are able to maintain stable coexistence
(MacArthur and Levins 1967, Pianka 1973, Schoener 1974, Chesson 1985). By exhibiting varying activity patterns in time, the frequency of interspecific encounters with sympatric species competing for the same resource or space is reduced (Kronfeld-Schor and Dayan 2003). This form of niche partitioning may occur through variation in phenological events, as in the contrasting seasonal activity of highly cryptic bumble bee species (Scriven et al. 2016). Scriven et al. (2016) found, through mitochondrial DNA sequencing, that Bombus magnus is reproductively active after the seasonal activity peaks of sympatric populations of B. lucorum and B. cryptarum. Patterns of phenological niche partitioning have also been exhibited by coexisting mildew species, dung inhabiting flies and beetles, adult damselflies, and frogs (Filip et al. 2012, Heard et al. 2015, Hamelin et al. 2016, Sladecek, Segar, et al. 2017, Sladecek,
Sulakova, et al. 2017). Patterns of temporal niche partitioning may also emerge at finer scales.
More specifically, species may partition their activity within the 24-hour diel cycle. Differences in the daily periodicity by similar organisms is represented in various communities. For example, within an assemblage of bats in a water-stressed environment, temporal partitioning between species occurs in their use of water holes with low spatial accommodation, thus facilitating their continued coexistence (Adams and Thibault 2006). Other groups of organisms that exhibit contrasting daily activity patterns include ants, frogs, rodents, and large terrestrial mammals
3 (Castro-Arellano and Lacher 2009, Stuble et al. 2013, Bardier et al. 2014, Ikeda et al. 2016). It is evident that through these varying niche differentiation strategies organisms can persist in competitive environments.
Climate Change Impacts on Ecological Interactions
Recent anthropogenic climate change poses a global threat to biodiversity (Thomas et al.
2004, Bellard et al. 2012). From 1850 to 2012, the globally averaged trend of land and ocean surface temperatures suggests a warming of 0.85°C, and global circulation models predict additional warming to exceed 1.5°C by the end of the 21st century (IPCC 2014). In response to this climate change, species of diverse taxa are altering their geographical ranges and seasonal timing of life-history events to avoid harsh environments (Walther et al. 2002, Parmesan and
Yohe 2003, Root et al. 2003, Perry et al. 2005, Menzel et al. 2006, Parmesan 2006, Primack et al. 2009). Patterns of shifting activity have also been documented to occur within the diel scale.
Diverse species, including mammals, birds, and social insects, have exhibited this behavioral shift of daily activity (Fraser et al. 1993, Paise and Vieira 2006, Kasper et al. 2008, Cid et al.
2015, Reddy et al. 2015, Silva et al. 2015). While at the population level, these ecological shifts facilitate avoidance of harsh environments, there may be extended consequences in terms of a species community as a whole. Because not all species within an ecosystem respond the at the same rate, community-wide synchrony of ecological interactions are disrupted (Harrington et al.
1999, Voigt et al. 2003, Tylianakis et al. 2008, Gilman et al. 2010, Donnelly et al. 2011). In fact, these biotic, indirect influences are an important mechanism leading to local extinctions in contrast to that of the direct abiotic mechanisms of climate change (Cahill et al. 2012, Ockendon et al. 2014).
4 An alternative to ecological shifts as a means of persistence in the face of novel climates may be adapting through genetic changes or acclimating through phenotypic plasticity
(Hoffmann and Sgró 2011). Given the current rate of environmental change, many organisms lack the capacity to genetically adapt at a pace matching recent and projected change (Merilä
2012). Therefore, acclimation through plasticity is an important mechanism mitigating the consequences of a changing climate (Przybylo et al. 2000, Price et al. 2003, Réale, Berteaux, et al. 2003, Réale, McAdam, et al. 2003, Gienapp et al. 2008). Phenotypic plasticity refers to the range of physiological or morphological states expressed by a single genotype in response to environmental variation (Bradshaw 1965, Crocker and Hunter 2018). In predicting the long-term effects of climate change on a population, knowledge of an organisms’ capacity to exhibit plasticity across multiple generations becomes a relevant topic. Transgenerational plasticity
(TGP) is the interaction of the environment experienced by the parent with the phenotype expressed by the respective offspring (Fox and Mousseau 1998). In TGP, parents utilize predictive environmental cues received prior to copulation to prime their offspring for unfavorable conditions. Understanding the transgenerational influence of the environment allows for a realistic understanding of a population’s resiliency to projected environmental shifts in the future (Hoffmann and Sgró 2011).
Empirical evidence of TGP in response to environmental perturbations associated with climate change is taxonomically diverse (Salinas et al. 2013). For example, several annual plant species exhibit TGP in response to drought stress (Riginos et al. 2007, Sultan et al. 2009,
Herman et al. 2012). Drought stressed plants of Polygonum persicaria, a habitat generalist, and
P. hydropiper, a moist-habitat specialist, respectively produced seedlings with extended and reduced root system development (Sultan et al. 2009). These effects of TGP often persist and
5 accumulate across multiple generations (Riginos et al. 2007, Herman et al. 2012). Evidence of
TGP in response to altered precipitation has also been exhibited in the American dog tick - the relative humidity experienced by the mothers influenced the larvae’ ability to absorb water vapor
(Yoder et al. 2006). Combating shifting CO2 levels through TGP has been observed in oysters and fish (Miller et al. 2012, Parker et al. 2012). CO2 exposed adult oysters, for instance, produced larger, CO2 resilient larvae with increased developmental rates (Parker et al. 2012).
Likewise, juvenile anemonefish exhibit decreases in length, weight, condition, and survival when exposed to elevated CO2 levels, unless their parents were also exposed to the same conditions
(Miller et al. 2012). Other examples include offspring toxicant tolerance after maternal exposure in bryozoans (Marshall 2008), modification of offspring size due to food limitations in the maternal environment of guppies (Bashey 2006), and offspring development with varying parental exposure to salinity in starfish (Hintz and Lawrence 1994).
Even more abundant are studies that examine the capacity of organisms to exhibit TGP in response to thermal environmental cues (reviewed in Donelson et al. 2017). In these studies, offspring whose parents were exposed to experimentally increased temperatures, exhibit modified life history traits favorable for increased temperatures. Such traits include increased developmental timing and growth rates, as seen in marine sticklebacks and butterflies (Steigenga and Fischer 2007, Salinas and Munch 2012), reduced egg and larval sizes in reef-building corals and butterflies (Fischer et al. 2003, Putnam and Gates 2015). Further, exposure of adults to increased ambient temperature has resulted in offspring with increased thermal tolerance as exhibited by springtails and polychaetes (Massamba-N’Siala et al. 2014, Zizzari and Ellers
2014). The rate of warming across generations may be an important parameter influencing TGP.
Donelson et al. (2016) demonstrated different transgenerational effects between a rapid and
6 gradual increase of 3°C over two or one generations, respectively. Those exposed to gradual temperature increases across generations exhibited greater plasticity of clutch and offspring size.
The Burying Beetles
Nicrophorine burying beetles of the family Silphidae exhibit unique reproductive behavior that requires the acquisition of an ephemeral resource. This genus is made up of around
75 different species with populations distributed in Europe, Asia, and North America (Peck and
Kaulbars 1987, Sikes et al. 2002). In order to reproduce, burying beetles must locate and secure a small vertebrate carcass that they will subsequently bury and prepare as a feeding resource for their developing larvae (Pukowski 1933, Scott 1998). From as far as several kilometers (Petruska
1975), adult burying beetles locate carrion through highly sensitive chemoreceptors that detect
Sulphur-containing chemicals characteristic of freshly decaying carcasses (Abbott 1927, Boeckh
1962, Ernst 1972, Kalinová et al. 2009). This is often accomplished in as little as one day after the demise of their resource (Conley 1982). Upon the discovery of a suitable carcass, if a female is not already present, males attract a mate through the emittance of a pheromone (Bartlett
1987a, Eggert and Müller 1989, Eggert 1992, Scott 1998, Haberer et al. 2008). The breeding pair then work together preparing the carcass for reproduction by moving it to a suitable burial spot, removing its hair or feathers, and depositing oral and anal antimicrobial secretions on its surface to reduce carcass decomposition (Milne and Milne 1976, Scott 1998, Suzuki 2001, Hoback et al.
2004, Rozen et al. 2008, Hall et al. 2011). During the preparation process, the carcass is formed into a brood ball and is simultaneously buried—either underground or beneath a layer of leaf litter—so as to conceal it within a breeding chamber (Pukowski 1933, Milne and Milne 1976,
Scott 1998).
7 Depending on the size of the carcass, females may lay anywhere between 10 to 30 eggs in the adjacent soil following carcass burial (Müller et al. 1990, Trumbo 1994, Nagano and
Suzuki 2007). Once the eggs have hatched, one or both parents may rear the larvae from the prepared carcass by regurgitating partially digested contents of the carcass to the larvae
(Pukowski 1933, Trumbo 1994, Xu and Suzuki 2001, Smiseth and Moore 2002). There are species-specific differences in obligate versus facultative parental care behavior, with extended implications for larval survival and fitness (Trumbo 1992, Capodeanu-Nägler et al. 2016). The emergence of this rare exhibition of extended bi-parental care, characteristic of the Nicrophorine genus, is thought to be the evolutionary culmination of scramble competition for ownership of an unpredictable, highly-nutritious resource (Pukowski 1933, Milne and Milne 1976, Anderson
1982, Trumbo 1994, Eggert and Müller 1997, Scott 1998, Xu and Suzuki 2001).
Ecological niche partitioning is an important factor mediating the persistence of sympatric species of burying beetles (Scott 1998). Differentiation of the carrion niche, for instance, has been documented to occur based on carcass size or type (Scott 1998). For example, larger beetles, such as N. orbicollis, are better able to manage larger carcasses while, smaller species, such as N. defodiens, are better equipped to manage small carcasses (Trumbo 1990a). However, burying beetles often exhibit overlap in their preference for a specific carcass size class. For instance, populations of N. maculifrons, N. quadripunctatus, and N. vespilloides do not differ in their preference for small or medium sized carcasses (Ohkawara et al. 1998). Nicrophorous investigator was also documented to exhibit preference for carcasses of intermediate size (Smith and Heese 1995, Smith and Merrick 2001). Divergence of the type of resource base has been documented in burying beetle communities. Interestingly, while populations of N. investigator found in the intermountain west feed primarily on small rodents (Smith and Merrick 2001), those
8 of the same species, co-occurring with N. defodiens in the Pacific northwest feed primarily on salmon, while N. defodiens feeds primarily on shrews and songbirds (Hocking et al. 2006, 2007).
One Nicrophorus species, N. pustulatus, has even exhibited behavioral adaptations allowing it to exploit reptilian eggs as a resource for breeding (Smith et al. 2007). Such niche use differences may serve as mechanisms for reducing food source and breeding resource competition with sympatric species.
Spatial niche partitioning among burying beetle species occurs through contrasting habitat selectivity (Scott 1998). The composition and texture of soil and land-use intensification are important habitat features that influence burying beetle distribution (Muths 1991, Scott 1998,
Bishop et al. 2002, Looney et al. 2009). Differences in climatic adaptations between N. orbicollis and N. defodiens populations in northern Michigan explain differences in their spatial abundance
(Wilson et al. 1984). Additionally, species-specific associations with land cover types reveal differential space-use patterns (Beninger and Peck 1992, Beninger 1994, Trumbo and Bloch
2000, Wilhelm et al. 2001, Urbański and Baraniak 2015, Leasure 2017, Leasure and Hoback
2017). Specifically, species including N. orbicollis and N. pustulatus are forests specialists, while species such as N. marginatus are open meadow specialists (Anderson 1982, Beninger and Peck
1992, Trumbo and Bloch 2000). In contrast, species including N. americanus and N. tomentosus are habitat generalists and can be found in meadows or open-canopy forests (Anderson 1982,
Beninger and Peck 1992, Trumbo and Bloch 2000, Leasure 2017, Leasure and Hoback 2017).
Examples of temporal niche partitioning of the small carrion niche facilitated by varying seasonal or daily activity patterns are evident in Nicrophorine populations. Studies utilizing pitfall trap data to measure species abundances over a seasonal time-scale show distinct fluctuations that differ between species (Anderson 1982, Wilson et al. 1984, Trumbo 1990b,
9 Beninger and Peck 1992, Beninger 1994, Ohkawara et al. 1998, Nagano and Suzuki 2003,
Mullins et al. 2013, Owings and Picard 2015). For example, while populations of N. sayi are active in the late spring, sympatric populations of N. tomentosus are thought to be active in the late summer to early fall (Anderson 1982, Wilson et al. 1984, Trumbo 1990b, Beninger and Peck
1992, Beninger 1994). Differences in the seasonal abundances of species often occur due to differences in emergence times and reproductive maturity, but seasonal reproductive overlap does occur (Scott 1998). Variation in daily activity patterns within burying beetle communities have also been documented using pitfall trap data (Wilson et al. 1984, Ohkawara et al. 1998,
Bedick et al. 1999). Species including N. tomentosus and N. marginatus are thought to be diurnal, while N. orbicollis are nocturnal (Wilson et al. 1984, Bedick et al. 1999). However, lacking in the current literature are more controlled and holistic accounts of the daily activity patterns of Nicrophorine communities thus restricting interpretations of daily temporal niche use.
While research on the behavioral ecology of burying beetles is vast, there are few studies that seek to understand the thermal ecology of this genus. Merrick and Smith (2004) explored the thermoregulatory abilities of three Nicrophorine species (N. hybridus, N. guttula, and N. investigator). In this study, beetles with larger body sizes were found to better maintain higher thoracic temperatures than environmental temperatures during flight (Merrick and Smith 2004).
Merrick and Smith (2004) also explored temperature as it relates to the daily activity of burying beetles and found where operative temperatures (i.e., the thermal environment an organism experiences) were high, burying beetle activity was low. Contrasting patterns emerged in a study by Nisimura et al. (2005), that attributed low temperatures as a suppressing factor in the activity patterns of burying beetles. One study explored the thermal tolerance of a species active in the spring and autumn in northern Taiwan and found at temperatures exceeding 26°C, the mortality
10 rates reach 100% (Hwang and Shiao 2011). While these studied allude to the direct impact of temperature on the daily activity and longevity of burying beetles, it is unknown if burying beetles are able to compensate through transgenerational responses in activity and reproductive biology. These questions become especially pertinent for species that are reproductively active in the warmest months of the year and exhibit diurnal activity patterns within geographical ranges expected to experience substantial climatic shifts.
Project Goals
This thesis is an effort to increase our understanding of how burying beetle persistence is influenced by competitive interactions and climatic variation. While there is evidence of spatial and temporal niche differentiation among burying beetles, there has been no synthesis of both space-use and daily activity patterns collected at a fine scale within speciose Nicrophorine communities. Chapter two addresses whether burying beetle species partition space and time as means of coexistence. Both the spatial distribution and daily temporal activity patterns are measured for five species of burying beetles co-occurring at a tallgrass preserve in north-central
Oklahoma. Furthermore, little is known about the thermal ecology in burying beetles including behavioral and physiological responses to lethal temperatures. Chapter three addresses the capacity of a burying beetle species, N. marginatus, to persist through projected climatic change.
Specifically, transgenerational effects of varying temperatures are tested by monitoring offspring morphological and life-history traits in response to parental thermal environment. Additionally, the daily activity patterns are measured within and between generations at varying temperature treatments. If the coexistence of sympatric burying beetle species is maintained, in part, by temporal niche variation, then projected temperature increases that may alter species’ activity patterns could compromise their persistence. Additionally, documenting the capacity of burying
11 beetles to exhibited thermal TGP will allow for a better understanding of their resilience to projected climate change models.
Studies that explore niche use patterns and climate change responses give light to our understanding of the decline and fate of threatened species. Direct competition among congeners is hypothesized as a factor in the decline of the endangered American burying beetle (N. americanus Oliver; Sikes and Raithel 2002). This species, federally listed in 1989, has declined in its geographic extent from 36 U.S. states to eight. Understanding the specific mechanisms behind facilitating or hindering the persistence of rare species’, including competitive interactions, can inform conservation strategies for protecting threatened species. Further, exploring the adaptive capacity of organisms in light of climate change at a local scale can help predict macroecological trends in biodiversity.
12 CHAPTER 2 – SPATIO-TEMPORAL NICHE USE PATTERNS OF SYMPATRIC NICROPHORUS SPP.
Introduction
Ecological niche partitioning emerges as the mediating factor in the high-stakes contest for access to shared resources (Hutchinson 1957). Theory posits that in order for ecologically similar species to avoid competitive exclusion, they must utilize their essential resources differently (Gause 1932, Hardin 1960). Therefore, coexistence among similar organisms is maintained through the distinction of a species’ resource niche. Such differences may occur through contrasting resource requirements; however, for species that overlap in their resource use, differential activity in space or time may serve as a means for reducing competitive interactions (Hardin 1960, Pianka 1973, Schoener 1974).
Examining resource allocation through contrasting use of space and time addresses how similar species avoid competitive exclusion. The current understanding of spatial niche partitioning is well established. Classic examples include MacArthur’s warblers that occupy distinct foraging locations on trees (MacArthur 1958), or Schoener’s Anolis lizards that spatially segregate their habitat according to perch height and diameter (Schoener 1968). While these examples were a primary focus in establishing the niche framework in ecology, more recent examples of spatial niche partitioning are numerous (Juncos et al. 2015, Samra et al. 2015,
Borkowski and Skrzecz 2016, Estavo et al. 2017). Less understood, however, is how species obtain ecological separation through partitioning activity in time (Kronfeld-Schor and Dayan
2003).
Temporal niche partitioning represents an important mechanism by which similar species coexist – by exhibiting varying activity patterns in time, species sharing an essential resource
(e.g. food) can avoid competitive encounters (MacArthur and Levins 1967, Schoener 1974,
13 Carothers and Jaksić 1984, Chesson 1985, Kronfeld-Schor and Dayan 2003). This form of resource partitioning may occur through variation in phenological events such as documented for three cryptic, co-occurring bumblebee species (Scriven et al. 2016), or though contrasting daily activity patterns as seen through segregated foraging times in a deciduous forest ant community
(Stuble et al. 2013). Though exploring temporal activity patterns gives further insight into the persistence of competing species, it is worth exploring both temporal and spatial characteristics in concert to gain a more holistic understanding of how species persist in competitive environments (Pianka 1973, Schoener 1974).
Burying beetles (Silphidae: Nicrophorus) exhibit unique reproductive behavior that is entirely dependent upon a carrion resource. To successfully reproduce, breeding pairs of burying beetles must locate a small vertebrate carcass to prepare as food for their developing larvae
(Pukowski 1933, Scott 1998). Given that carrion resources are utilized by a variety of necrophilous invertebrate and vertebrate scavenger species (Putman 1978, Devault et al. 2003,
2004, Barton et al. 2013), and the ephemeral nature of this resource (Finn 2001), burying beetles must then undergo intense competition to secure a carcass for reproduction. This scramble competition for high-value resources (Trumbo 1990c, Lane et al. 2010) represents a unique opportunity for investigating the mechanisms necessary for species’ persistence in the ecological context of niche segregation.
Although how burying beetle species persist in Nicrophorine-rich communities is unknown, documented examples of spatial and temporal patterns indicate differential use of these niche dimensions. For example, different habitat characteristics predict the spatial distribution of burying beetle populations, suggesting spatial niche partitioning may occur at relevant scales. Specifically, species that are commonly found in forested areas include N.
14 defodiens, N. orbicollis, N. sayi, and N. pustulatus (Anderson 1982, Beninger and Peck 1992,
Beninger 1994, Trumbo and Bloch 2000, Wilhelm et al. 2001). In contrast, individuals of N. investigator, N. vespillo, and N. marginatus are significantly associated with open meadows and fields (Anderson 1982, Smith and Heese 1995, Trumbo and Bloch 2000, Wilhelm et al. 2001,
Urbański and Baraniak 2015), while N. americanus and N. tomentosus, habitat generalists, are found in both open meadows and open-canopy forests (Anderson 1982, Beninger and Peck 1992,
Trumbo and Bloch 2000, Leasure 2017, Leasure and Hoback 2017).
Temporally based resource partitioning between burying beetle species is evident through both phenological and diel patterns detected via capture timing data (Anderson 1982, Wilson et al. 1984, Trumbo 1990b, Ohkawara et al. 1998, Nagano and Suzuki 2003, Mullins et al. 2013,
Owings and Picard 2015). Such species-specific seasonal fluctuations in reproductive activity are well-documented. For instance, N. sayi is thought to be reproductively active in the late spring, while sympatric populations of N. orbicollis and N. tomentosus are active in the early summer and late summer to early fall, respectively (Anderson 1982, Wilson et al. 1984, Trumbo 1990b,
Beninger and Peck 1992, Beninger 1994). Further, previous studies that quantify daily activity in burying beetles through hourly trap checks, provide evidence for daily temporal niche partitioning (Wilson et al. 1984, Ohkawara et al. 1998, Bedick et al. 1999). Specifically, N. tomentosus is thought to be diurnal, while N. orbicollis, N. sayi, and N. americanus are thought to be nocturnal (Wilson et al. 1984, Bedick et al. 1999). To this point, however, there has been no high-resolution, empirical examination of the daily activity of burying beetles. Further, there has been no synthesis of how such patterns relate to space use in a speciose Nicrophorine community where competition for the carrion resource is assumed to be intense.
15 The goals of this study were to 1) examine, at a fine scale, the spatial distribution patterns of five sympatric species of Nicrophorine burying beetles at a tallgrass preserve in north-central
Oklahoma, and 2) empirically measure their daily temporal activity patterns to investigate whether species in this genus partition space and time as mechanisms for coexistence. In order to reduce congeneric competitive interaction, it is possible that sympatric burying beetle species have coopted distinct spatio-temporal niches. Some Nicrophorine burying beetles are known to prefer distinct habitats, but no study has explicitly examined multi-species communities to understand how space use patterns may represent a dimension of resource segregation.
Additionally, pair-wise comparisons of daily activity patterns may demonstrate the extent of temporal niche segregation and overlap, which may explain the space use patterns that emerge across the landscape.
Methods
Field Collection and Laboratory Culture
During the summer months of 2014-2017, we conducted a survey of Nicrophorine burying beetle (N. americanus, N. marginatus, N. tomentosus, N. orbicollis, and N. pustulatus) abundance and distribution at the Nature Conservancy’s Tallgrass Prairie Preserve (TGPP) in
Osage County, Oklahoma (36o49’N, 96o23’W). Across the extent of the 16,045-hectare nature preserve, forty above-ground baited traps were placed at 2,000 m intervals on a grid, using trap designs modified from Leasure et al. (2012). Traps were baited with aged chicken liver and checked for three consecutive mornings in accordance with the U. S. Fish & Wildlife Service
(USF&WS) trapping protocols. Trapping occurred over the span of 16 days during early July each year and consisted of four trapping cycles in total, with 10 sample sites trapped
16 simultaneously. Upon checking traps each morning, the number of each species of Nicrophorus burying beetles was recorded. During the 2017 active season, individuals of all five species were temporarily brought into the lab for locomotion activity measurements. Prior to these activity trials, beetles were housed in aquaria with peat moss substrate and were separated by species and sex. N. americanus were individually housed in ventilated acrylic containers. All beetles were provided with small 1.0 g aliquots of raw pork meat and fresh water ad libitum, and maintained in a 14:10 Light/Dark photoperiod. N. americanus were collected under the authority of the
USFWS Endangered Species Research and Recovery Permit TE 170625-0 issued to DRH and
CLH.
Space use modeling
Prior to integrating field collection data into a GIS, all raw abundance data were converted to mean trap-rates (beetles trap-night-1) for each sampling site. We then incorporated these trap-rate data into the attribute table of a GIS (ArcMap desktop version 10.3; ESRI,
Redlands, CA USA) and used these values to model the core range of each of the five species.
We estimated core ranges using the kernel density estimate function in the ArcMap Spatial
Analyst Toolbox. We parametrized the kernel density output cell size to 50.58 m, which was calculated as the shorter of the width or height of the output extent in the output, divided by 250
(default ArcMap setting), and chose a planar method for density estimates due to the small geographic scale of the model. The absolute output extent was defined as the preserve boundaries. We then calculated 50% core ranges using the isopleth function in Geospatial
Modelling Environment (GSM; Beyer 2012) software. We calculated the area (km2) for all isopleths in GSM, and then exported shapefiles of these core areas of abundance for use in subsequent spatial overlap analysis in ArcMap. We examined clustering of burying beetle
17 abundances across the landscape using spatial autocorrelation analysis conducted in the spatial statistics toolbox in ArcMap, and calculated descriptive statistics and conducted pairwise species comparisons of core ranges to examine patterns of spatial overlap in JMP Pro version 13.0.0
(SAS Institute Inc. Cary, NC USA).
Temporal Niche Analysis
The activity patterns of all five species were measured using Trikinetics, Inc., (Waltham,
MA, USA) activity monitors (Pfeiffenberger et al. 2010). Each activity monitor contains 32 channels each with a photo-eye that, when disrupted, documents a single activity event.
Individual beetles were placed in 2.5 x 20 cm clear acrylic tubes that were loaded into the activity channels. On opposite ends of each tube, fresh food and water were available to the insects ad libitum. Activity trials consisted of a 24-hour tube-enclosure acclimation period and three 24-hour periods of activity data collection. Trials were conducted in controlled temperatures of 25°C (+/- 0.5°C) on a 14:10 Light/Dark photoperiod. All individual that underwent activity trials were assigned a unique alpha-numeric identifier that included their sex and species.
To determine when each species exhibits the highest daily activity, total counts of activity for individuals were binned into 12 consecutive 2-hour time-blocks. Time blocks were compared using Kruskal-Wallis rank sum tests. Post-hoc analyses were performed using nonparametric comparisons for each possible pair using the Wilcoxon method. Time-block comparisons were made in JMP Pro version 13.0.0 (SAS Institute Inc. Cary, NC USA).
To determine the temporal niche of sympatric burying beetle species, we quantified the extent of temporal niche overlap between each possible species pair. To do so, the total counts of activity for individuals were first binned into 15-minute time intervals within the first 24-hour
18 data collection period. An individual was considered “active” within a single interval if it had one or more total count of activity within those 15-minutes. The number of active individuals for each 15-minute interval was extrapolated to create activity distributions for each species through kernel density estimates made using the Overlap package (Meredith and Ridout 2017) in R 3.4.2.
In this context, estimates of kernel density describe the probability of an event of activity occurring at any given 15-minute time interval. Temporal overlap was then determined by calculating the overlap coefficient, D, of activity distributions following the procedure developed by Ridout and Linkie (2009). The nonparametric estimator of overlap for circular distributions,
D4, developed by Schmid and Schmidt (2006) was used for all 10 pair-wise comparisons.
Confidence intervals were determined using the basic0 output generated through 10,000 bootstrapped samples following Meredith and Ridout (2017).
Results
We collected 3,119 total Nicrophorine burying beetles over the course of the four years of the study (Table 1), with the mean trapping rates for all five species differing between sites and years. The most abundant burying beetle species at the study site was N. marginatus, with a mean 4-year trap rate of 3.32 ± 2.78 SD beetles trap night-1. N. tomentosus were the rarest species, with only 62 beetles collected and an overall trap rate of only 0.11 ± 0.16 SD beetles trap night-1. The other three species’ trap-rates were intermediate to these, and varied between years.
Space use
As with trap-rates, space use in Nicrophorine burying beetles differed between species and varied in both the size of their core ranges (Table 1), the heterogeneity of their local
19 distribution and the degree to which each species’ core range overlapped with those of others
(Table 2). Two species abundances exhibited significant spatial clustering of abundances on the landscape (N. americanus and N. marginatus), while other species were more homogenously distributed. N. marginatus abundances were associated with open grassland settings, contrasting most strongly with the space use pattern of N. orbicollis, which was restricted in spatial extent to the few forested areas of the study site (Fig. 1). N. marginatus exhibited consistently low spatial overlap with all other species including N. americanus (Fig. 2). Pairwise comparisons of mean annual spatial overlap demonstrated varying overlap values by year (Table 3), however, they highlight greater spatial segregation between N. marginatus and all species including N. americanus (Fig. 3)
Temporal Niche Patterns
In total, 29 individual N. americanus, 71 N. marginatus, 33 N. orbicollis, 50 N. pustulatus, and N. tomentosus were used to estimate daily activity patterns and temporal niche segregation. Within-species time block comparisons showed that the activity is highest for N. americanus in the early mornings, between 4:00am and 6:00am. Nicrophorus marginatus and N. tomentosus overlap in their periods of highest activity between 4:00pm and 8pm, as do N. orbicollis and N. pustulatus between 10:00pm and 12:00am (Table 4 and Fig. 4).
Of the 10 species pairs, the overlap coefficient, D, indicated low (< 0.60) overlap for two species combinations – the activity distribution of N. tomentosus appeared segregated from that of N. orbicollis and N. pustulatus (D = 0.5502, D = 0.4536; Table 5). Further, we found high temporal overlap coefficient values (> 0.75) for 2 species pairs: N. pustulatus with N. orbicollis, and N. americanus with N. orbicollis, indicating likely temporal niche overlap (D = 0.8693 and D
20 = 0.8024, respectively; Table 5). The remaining six species pairs exhibit lower temporal niche overlap (0.60 < D < 0.75).
Discussion
For burying beetles abundant in the speciose TGPP community, competition is mediated, in part, by temporal and spatial segregation patterns. While all five species exhibited low spatial overlap, evidence for contrasting space-use patterns is most notable between N. marginatus and all other species. This spatial divergence by N. marginatus suggests low competitive pressure for the carrion resource and may explain why this species appears to be a temporal niche generalist as documented here. Further, N. marginatus exhibited high temporal overlap with N. tomentosus suggesting that the exploitation of contrasting spatial niches may facilitate their coexistence.
Pairwise interspecies overlap percentages indicate low spatial overlap between all but two species pairs. N. pustulatus and N. tomentosus exhibited relatively high percent overlap, however, this pattern was highly variable by year. Nonetheless, our findings suggest that this overlap may be mediated by their contrasting daily activity patterns that indicate temporal niche divergence.
Where the measured spatial and temporal niche patterns suggest direct competition is between that of N. pustulatus and N. orbicollis. These two species exhibited both a high space- use overlap percentage as well as a high temporal overlap coefficient. While the similarities in the spatial and temporal ecology of these species imply a negative competitive interaction, N. pustulatus has exhibited a remarkable shift in its reproductive resource (Smith et al. 2007). This species is unique in that it has evolved behaviorally to exploit reptilian eggs as a reproductive resource (Smith et al. 2007). The spatial and temporal overlap between N. pustulatus and N.
21 orbicollis documented here, coupled with the intense competition associated with carrion, could have been the selective force driving this resource shift. However, future work should assess whether the TGPP population of N. pustulatus exhibits this behavioral resource shift as there is evidence for community-specific resource shifts in burying beetles. For instance, while populations of N. investigator co-occurring with N. defodiens in Coastal British Columbia feed primarily on salmon (Hocking et al. 2006, 2007), those found in the western U.S. feed primarily on small rodents (Smith and Merrick 2001).
The current understanding of the daily activity patterns of burying beetles has been based on the timing of individuals captured in pitfall traps (Wilson et al. 1984, Ohkawara et al. 1998,
Bedick et al. 1999). This is the first study to experimentally measure the 24-hour daily activity patterns of these five species of North American Nicrophorus beetles. The daily activity patterns predicted by previous field capture studies are consistent with the findings of the current study for N. tomentosus, that exhibited diurnal patterns, and for N. pustulatus and N. orbicollis, who both exhibited distinctly nocturnal patterns (Wilson and Fudge 1984, Ratcliffe 1996). However, these data do suggest that N. marginatus and the endangered N. americanus activity patterns are not what has been previously thought; these two species were thought to exhibit diurnal and nocturnal patterns, respectively (Ratcliffe 1996, Bedick et al. 1999). While our data do indicate diurnal activity in N. marginatus, there was a significant amount of activity exhibited by this species during the nocturnal time-blocks. Furthermore, for N. americanus, that exhibited primarily nocturnal behavior, an activity peak was detected between 6:00am and 8:00am, contrasting with that of previously published work. These findings have direct conservation implications. For instance, prescribed fire and grazing regimes, a common practice implemented within N. americanus critical habitats, can be scheduled so as to reduce interference with the
22 activity timing of this species. Additionally, the current USF&WS trapping protocol has no specification for when trap surveys begin (USF&WS 2018). If traps are checked prior to 8:00am, a critical time of N. americanus activity, trapping results may produce inaccurate presence/absence data.
Direct competition among congeners is one of the hypothesized reasons for the decline of the N. americanus (Sikes and Raithel 2002). The current study is the first to directly examine the competitive interactions of N. americanus present in a congeneric-rich community. Here we demonstrate that competition for the carrion resource is mediated by differential space-use and temporal activity patterns. Sikes and Raithel (2002) speculate that N. americanus could be competing directly with N. orbicollis due to their similar ecologies. However, our results reveal that, while these two species exhibit temporal niche overlap, their space use patterns are segregated. Further, patterns of spatial or temporal niche partitioning are evident among N. americanus and all other species abundant at the TGPP, suggesting that direct competition is not supported as an explanation for the decline of this species. Therefore, future work should explore the alternative decline hypotheses including increased pesticide exposure or habitat loss (Sikes and Raithel 2002).
These findings reveal an important interplay of space-use and temporal activity allowing for the differential exploitation of a shared ephemeral resource amongst congeners. Overall, the findings of this study contribute to the broader understanding of space and time as important niche dimensions and indicate their role in mediating direct competition among sympatric burying beetle species. Future work should aim to gain further resolution of the burying beetle ecological niche, including a comprehensive assessment of both the phenological and trophic niche patterns of the populations occurring within the north central Oklahoma community.
23 Tables
Table 1: Capture data and core range estimates for five sympatric species of Nicrophorus burying beetles collected each July over four years at the Nature Conservancy’s Tallgrass Prairie Preserve in Osage County, Oklahoma, USA. N. marginatus was the most common species, with abundances concentrated in open grassland sites. Its core range, like that of the other five species, was highly variable between years. The core range of N. americanus decreased during a year of low abundances, then rebounded during subsequent years when abundances increased.
Core Trap- Species Year Qty. range rate (km2) 2014 237 1.02 46.36 2015 30 0.21 12.59 N. americanus 2016 403 3.33 20.01 2017 226 1.77 33.11 2014 622 2.68 7.3 2015 146 1.01 35.87 N. marginatus 2016 890 7.36 22.36 2017 286 2.23 30.46 2014 43 0.19 27 2015 9 0.06 3.68 N. orbicollis 2016 26 0.21 25.27 2017 8 0.06 28.17 2014 16 0.04 56.9 2015 24 0.17 25.52 N. pustulatus 2016 57 0.47 5.77 2017 34 0.27 28.53 2014 12 0.05 27.92 2015 5 0.03 10.25 N. tomentosus 2016 42 0.35 21.47 2017 3 0.02 3.41
24
Table 2: Spatial autocorrelation scores and core range overlap estimates for five species of Nicrophorine burying beetles collected at The Nature Conservancy's Tallgrass Prairie Preserve over four years. The space use patterns of two species, N. americanus and N. marginatus, exhibited significant spatial clustering on the landscape during two different years of the study. N. marginatus, a grassland specialist, exhibited consistently low levels of spatial overlap with all other species including N. americanus, a habitat generalist.
Year Moran's I Z score P % overlap 2014 0.059 0.770 0.441 21.8% 2015 0.331 3.056 0.002 16.0% 2016 0.234 2.291 0.022 10.3% N. americanus 2017 0.101 1.116 0.265 30.2% 2014 0.258 3.197 0.001 4.8% 2015 -0.069 -0.369 0.712 8.9% 2016 0.303 2.861 0.004 11.0% N. marginatus 2017 0.091 1.012 0.312 12.4% 2014 0.043 0.625 0.532 16.9% 2015 -0.002 0.379 0.705 37.5% 2016 0.146 1.556 0.120 21.7% N. orbicollis 2017 -0.021 0.041 0.968 25.8% 2014 -0.076 -0.426 0.670 20.6% 2015 0.024 0.424 0.671 11.4% 2016 0.024 0.731 0.465 42.2% N. pustulatus 2017 0.078 0.916 0.359 25.6% 2014 0.152 1.506 0.132 28.1% 2015 0.038 0.547 0.584 8.0% 2016 0.183 1.818 0.069 24.7% N. tomentosus 2017 0.005 0.295 0.768 50.0%
25
Table 3: Comparison of interspecies overlap for each species pair over the four years. Species combo represents the percent of the first species’ core range overlapping with the second species’ core range. For each species pair, there is high variability in percent overlap by year, and the overall overlap values are relatively low. (ABB = N. americanus; MRG = N. marginatus; ORB = N. orbicollis; PUS = N. pustulatus; and TOM = N. tomentosus). Species Combo Year Mean Species Pair (Spp1 - Spp2) 2014 2015 2016 2017 Overall Mean A-M 0.014 0.308 0.310 0.223 0.214 ABB - MRG M-A 0.088 0.108 0.278 0.242 0.179 A-O 0.281 0.141 0.005 0.504 0.233 ABB - ORB O-A 0.483 0.481 0.004 0.592 0.390 A-P 0.403 0.193 0 0.378 0.244 ABB - PUS P-A 0.329 0.095 0.002 0.439 0.216 A-T 0.175 0 0.094 0.103 0.093 ABB - TOM T-A 0.291 0 0.088 1.000 0.345 M-O 0.029 0.003 0.096 0 0.032 MRG - ORB O-M 0.008 0.024 0.085 0 0.029 M-P 0.037 0.153 0 0.114 0.076 MRG - PUS P-M 0.005 0.216 0 0.154 0.094 M-T 0.037 0.091 0.065 0.112 0.076 MRG - TOM T-M 0.01 0.32 0.068 1.000 0.349 O-P 0.183 0.995 0.228 0.439 0.461 ORB - PUS P-O 0.087 0.143 1.000 0.433 0.416 O-T 0 0 0.55 0 0.138 ORB - TOM T-O 0 0 0.647 0 0.162 P-T 0.404 0 0.688 0 0.273 PUS - TOM T-P 0.824 0 0.185 0 0.252
26
Table 4. Time blocks of highest and lowest activity for each species. Nicrophorus marginatus and N. tomentosus are most active between 4:00pm and 8:00pm during the lower activity blocks of N. orbicollis and N. pustulatus. The latter two species also overlap in their peak activity blocks between 10:00pm and 12:00am. Nicrophorus americanus is most active between 4:00am and 6:00am.
Maximum Activity Minimum Activity Time Block Species Mean SE H Species Mean SE H 6:00-8:00 MRG 53.92 4.50 262.71
MRG 76.38 5.53 262.71 8:00-10:00 PUS 20.40 4.76 767.81 MRG 55.89 4.09 262.71 10:00-12:00 PUS 18.49 4.80 767.81
ABB 33.81 3.86 541.09 ORB 4.970 1.94 711.37 12:00-14:00 PUS 13.94 3.70 767.81 ABB 58.05 7.31 541.09 14:00-16:00 PUS 17.88 4.47 767.81 MRG 120.92 5.52 262.71 ORB 6.22 3.00 711.37 16:00-18:00 TOM 84.98 4.91 610.51 PUS 10.45 2.20 767.81 MRG 110.12 5.19 262.71 ORB 7.01 3.32 711.37 18:00-20:00 TOM 76.01 4.6 610.51 PUS 15.61 4.02 767.81
20:00-22:00 ORB 22.4 4.95 711.37 22:00-24:00 PUS 330.51 14.25 767.81
24:00-2:00 ORB 4.97 1.94 711.37 2:00-4:00 TOM 18.2 2.61 610.51 ABB 61.73 5.01 541.09 MRG 64.94 4.70 262.71 4:00-6:00 TOM 23.19 3.74 610.51
27
Table 5: The overlap coefficient, D, and the upper and lower 95% confidence intervals for each possible species pair (n=10). The overlap coefficient was lowest between N. tomentosus and N. orbicollis; and N. tomentosus and N. pustulatus (bolded). Conversely, the highest observed temporal overlap coefficient value was between N. pustulatus with N. orbicollis indicating temporal niche overlap.
Estimate of Overlapping Lower 95% Upper 95% Species Pair D CI CI ABB - MRG 0.7113 0.6803 0.7510 ABB - ORB 0.8024 0.7621 0.8459 ABB - PUS 0.6722 0.6399 0.7140 ABB - TOM 0.6653 0.6337 0.6959 MRG -ORB 0.7293 0.7056 0.7586 MRG - PUS 0.6827 0.6633 0.7089 MRG - TOM 0.7273 0.7075 0.7503 ORB - PUS 0.8693 0.8365 0.8966 ORB - TOM 0.5502 0.5231 0.5839 PUS - TOM 0.4536 0.4350 0.4805
28 Figures
Fig 1: Map illustrating the spatial segregation between N. marginatus (yellow polygon) and N. orbicollis (green polygon) at the Tallgrass Prairie Preserve study site. N. marginatus’ core range was restricted to open grassland areas of the site, whereas the highest abundances and core range extent for N. orbicollis were restricted to the few forested areas at the site.
29
Fig. 2: Mean 4-year interspecies core range overlap between five sympatric Nicrophorine burying beetle species at the TNC Tallgrass Prairie Preserve study site in Osage County, Oklahoma. N. marginatus exhibited consistently lower space use overlap with the other four species (Mean = 9.1±3.1%), with all five burying beetle species rarely overlapping by more than 25% of their core ranges.
30 Percentage Overlap 1.0
0.8
0.6
0.4 Percentage Overlap Percentage 0.2
0.0
ABB - PUS ORB -PUS ABB - MRGABB - ORB ABB - TOMMRG - ORBMRG - PUSMRG - TOMORB - TOM PUS - TOM
Species Pair
Fig. 3: Pair-wise interspecies percent overlap highlighting the low spatial overlap of N. marginatus with all other species. With the exception of two species pairs, the spatial overlap between Nicrophorine species at the TGPP is relatively low. Spatial overlap is higher between N. orbicollis and N. pustulatus, as well as for N. pustulatus and N. tomentosus.
31
Fig. 4: The Kernel density estimates across the 24-hour diel cycle for all species. Activity measurements were recorded under a 14:10 Light:Dark photoperiod representing day and night. Shaded portions of the graph represent night, while unshaded represent day. N. tomentosus exhibited a distinct diurnal activity pattern, while N. orbicollis and N. pustulatus appear to be nocturnal. N. marginatus and N. americanus exhibited activity peaks in both the night and day hours.
32 CHAPTER 3 – THERMAL ENVIRONMENTAL CUES ON THE REPRODUCTIVE BIOLOGY OF NICROPHORUS MARGINATUS
Introduction
Since 1890, the Earth has warmed by 0.85°C, and global circulation models project an additional increase of 1.5°C by the end of the 21st century (IPCC 2014). While current biodiversity loss is attributed mainly to habitat destruction (Hoffmann et al. 2010), climate change is predicted to be a growing driver of species extinctions in the near future (Thomas et al.
2004, Pereira et al. 2010, Bellard et al. 2012). Further, the synergistic effects of both habitat loss and climate change are also expected to drive significant declines in biodiversity (Travis 2003,
Mantyka-Pringle et al. 2012). While a diverse set of species have already exhibited ecological shifts to escape harsh climates (Walther et al. 2002, Parmesan and Yohe 2003, Root et al. 2003,
Perry et al. 2005, Menzel et al. 2006, Parmesan 2006, Primack et al. 2009), it is important to assess the vulnerability of species that currently persist close to their physiological limits to ascertain species of high conservation priority (Dawson et al. 2011, Hoffmann and Sgró 2011).
To assess a species’ vulnerability to climate change-induced abiotic stressors, it is also critical to understand the physiological sensitivity and adaptive capacity of a species to respond to thermal stress (Williams et al. 2008, Chown et al. 2010, Hoffmann and Sgró 2011, Huey et al. 2012).
To prevent local extinctions, organisms may respond to environmental change by adapting to novel climates through genetic changes (Hoffmann and Sgró 2011, Gonzalez et al.
2013). While evidence for such rapid evolutionary change has been found in a number of taxa
(Hendry et al. 2008), many species lack the capacity to adapt at a rate matching the current pace of climate change (Merilä 2012). For such species, acclimation through plastic changes will serve as a buffer against the negative impacts of climate change (Przybylo et al. 2000, Price et al.
2003, Réale, Berteaux, et al. 2003, Réale, McAdam, et al. 2003, Gienapp et al. 2008). Further,
33 this phenotypic plasticity is thought to facilitate genetic change thus reducing extinction risks in unfavorable environments (Chevin et al. 2010, Kopp and Matuszewski 2013). The capacity of organisms to exhibit transgenerational plasticity (TGP), or plastic responses that occur across generations, is of interest when assessing the long-term effects of climate change (Salinas et al.
2013, Donelson et al. 2017). TGP represents how the environment experienced by one or both parents shapes the respective offspring’s reaction norm (Fox and Mousseau 1998). This phenomenon has been exhibited across taxonomic groups in response to a variety of environmental perturbations associated with climate change (reviewed in Salinas et al. 2013 and
Donelson et al. 2017).
Ambient temperature extremes are of particular concern for ectothermic animals whose thermoregulation is dependent on environmental conditions. Research addressing the influence of temperature on ectotherms has increased in light of recent climate change patterns (Deutsch et al. 2008, Sunday et al. 2011, 2014, Woods et al. 2015, Abram et al. 2017). TGP has specifically been identified as an important mechanism for overcoming predicted climate trends (Groeters and Dingle 1988, Fischer et al. 2003, Steigenga and Fischer 2007, Salinas and Munch 2012,
Massamba-N’Siala et al. 2014). In these studies, modified offspring phenotypes result from parental exposure to experimental warming treatments. For example, in marine sticklebacks, offspring whose parents were exposed to increased temperatures experienced increased growth rates when exposed to the same temperatures (Salinas and Munch 2012). Other modifications include reduced egg and larval sizes, as exhibited by reef-building corals and butterflies (Fischer et al. 2003, Putnam and Gates 2015). In environments of increased temperature and variable precipitation, a reduction in body size is selected for given its direct link to thermoregulation
(Gardner et al. 2011). Even more profoundly, offspring of thermally stressed parents have even
34 been documented to have increased thermal tolerances. This pattern was exhibited in springtails and polychaetes (Massamba-N’Siala et al. 2014, Zizzari and Ellers 2014).
Nicrophorine burying beetles play an important ecological role in the breakdown of organic material. Reproduction in burying beetles involves the acquisition of a small vertebrate carcass that is buried and prepared as food for their developing larvae (Pukowski 1933, Milne and Milne 1976, Scott 1998). Many Nicrophorine species exhibit obligate bi-parental care and have been documented to modulate brood characteristics in response to environmental cues
(Scott 1990, Scott and Traniello 1990, Trumbo 1991). For example, in response to limited resource availability, burying beetle parents have been documented to modulate brood size through infanticide (Bartlett 1987b, Trumbo 1990c, 2006, Robertson 1993). Further, in N. marginatus, parental exposure to high levels of conspecific density resulted in smaller broods with individuals of increased body size (Woelber et al. 2018). The results of these studies demonstrate that burying beetles modulate offspring characteristics to be favorable in their perceived environments. While the behavioral ecology of burying beetles is well studied, very little is known about their thermal ecology, and particularly, how thermal environments shape burying beetle reproductive biology and behavior.
In this study, the effect of temperature on the reproductive biology and movement activity is explored in N. marginatus, a Nicrophorine species abundant in north-central
Oklahoma. Given that this species is reproductively active in the warmest months of the year
(Mullins et al. 2013), exhibits diurnal activity patterns (Keller et al. in prep), and is abundant in open grassland habitats (Anderson 1982, Trumbo and Bloch 2000), N. marginatus are likely adapted to persist among high ambient temperatures. Yet, this region of North America is
35 expected to experience a warming trend of 1.67 - 2.78°C over the next 50 to 75 years (Oklahoma
Department of Wildlife Conservation 2016). If these projections surpass the thermal limits of N. marginatus, the ecologies specific to this species may present an evolutionary disadvantage.
To explore the capacity of this species to respond to projected temperature shifts via behavioral modifications and TGP, we assessed how the thermal environment influences rearing behaviors, reproductive success, and movement activity both within and across generations.
Additionally, we investigate the influence of parental thermal environment on brood size, the average individual size of offspring, and offspring sex ratio. By assessing these parameters, we tested the hypothesis that natural selection has selected for traits in this species that render it successful in increasing temperatures. If this is the case, then we expect minimal effects of temperature on reproductive behaviors, reproductive success, and movement activity. Further, we expect offspring of parents exposed to elevated temperatures to exhibit modified characteristics favorable in high thermal environments. If N. marginatus reaches its thermal capacity at the projected temperature trends, we alternatively expect modified reproductive behaviors, a decline in reproductive success, suppressed movement activity, and an absence of
TGP in the measured parameters.
Methods
Study subjects and field methods
N. marginatus were collected from the Nature Conservancy’s Tallgrass Prairie Preserve in Osage County, Oklahoma (36o49’N, 96o23’W). During the summer of 2018, individuals of N. marginatus were collected using above-ground bucket traps baited with aged chicken liver
(Leasure et al. 2012). Forty traps were placed at 2,000 m intervals across the extent of the 16187-
36 hectare nature preserve and were checked for three consecutive mornings in accordance with the
US Fish & Wildlife Service N. americanus trapping protocol. All beetles collected were brought back to the laboratory at the University of New Hampshire where they were housed individually in ventilated acrylic containers with peat moss substrate and were provided with food and water ad libitum, and maintained in a 14:10 Light/Dark photoperiod.
The ten-year (2008-2017) average daily minimum and maximum temperature for the active breeding season of N. marginatus (June-August) at the collection location ranged from
19.5°C to 31.8°C with the total average being 25.5°C (Foraker Mesonet Station, Osage County,
OK; https://www.mesonet.org/). Therefore, reflecting the historical temperature experienced by
N. marginatus in the wild, the baseline temperature for this experiment was 26°C. From the wild-caught population, approximately 100 breeding pairs were selected at random and were given a mouse carcass to rear the F1 generation at the baseline temperature. Following the culture breedings, the F1 adults were held at 26°C until the start of the experiment.
The Oklahoma region is expected to experience a warming trend of 1.67 - 2.78°C over the next 50 to 75 years (Oklahoma Department of Wildlife Conservation 2016). Using controlled environmental chambers, two transgenerational temperature treatments (see figure 1) were chosen to reflect these predicted trends at varying rates of increase across generations: 1) rapid increase of 1.5°C over one generation (26 to 27.5°C); and 2) incremental or step-wise increase of
0.5°C over two generations (26 to 26.5 to 27°C). Additionally, two control treatments were used:
1) Control A maintained a temperature of 26°C across three generations to account for confounding effects of generation or seasonality; and 2) to test whether parental exposure at
26.5°C (F2 step) or 26°C (F2 control) had an effect on the measured parameters of their offspring
37 at 27°C (F3), a subset of the control offspring were reared at 27°C in the third generation (26 to
26 to 27°C).
For each generation of all temperature treatments, 30 (±4) breeding pairs of N. marginatus were placed in 80 oz. acrylic breeding containers with a depth of approximately 6 cm of moistened peat moss and a single 27 (±2) g mouse carcass. All chambers were set to a 14:10
Light/Dark photoperiod. Prior to each generation round, breeding individuals were exposed to their rearing temperature for 7 days.
Reproductive behavior and plasticity of N. marginatus was quantified through the measurement of the following parameters: burial duration (hrs), breeding success (Y/N), brood size, individual offspring size and offspring sex ratio. Once parents were placed in breeding containers, burial progress was checked every hour. Breeding containers were thereafter checked daily for dispersed larvae. Once larvae dispersed from the brood chamber, individuals were quantified and transferred to fresh peat. Daily checks continued until all the offspring emerged as adults. As they emerged, offspring individuals were imaged, and placed in individual containers labeled with breeding identification, offspring number, and treatment condition. To proximate individual body size, the pronotum of all offspring were measured using ImageJ (version 1.51s; https://imagej.nih.gov/ij/), a public domain image analyzing software. For each breeding pair, the mean pronotum width of all offspring were used in the analysis.
To test whether temperature influences the movement activity of burying beetles, and to test for transgenerational plasticity, the activity of N. marginatus offspring were measured between breeding experiments. First, a subset of the F2 offspring of the F1 parents (26°C rearing temperature) were used to assess their movement activity in control (26°C) and elevated
(26.5°C) temperature treatments. Following activity trials, this generation was bred in the
38 respective control and elevated temperature treatments. A subset of the offspring (F3) from the
26°C and 26.5°C rearing environments were exposed to the elevated temperature treatment
(26.5°C) and their activity was measured. The mean activity counts in each treatment were measured using Trikenetics, Inc., (Waltham, MA, USA) activity monitors. Each 32-channel activity monitor uses a photo-eye that, when disrupted, documents a single count of activity of the contained beetle. For each treatment, a random sample of approximately 32 beetle individuals were placed in the Trikinetics, Inc., activity monitor that consists of clear plastic tubes that are loaded into the activity channels (Fig. 2). On opposite ends of each tube, fresh food and water was available to the insects ad libitum. Activity trials consisted of a 24-hour tube- enclosure acclimation period and three 24-hour periods of activity data collection. Trials were conducted in the respective treatment condition with a 14:10 Light/Dark photoperiod. All individual beetles that underwent activity trials were assigned a unique alpha-numeric identifier that included their sex, generation, and treatment condition.
Statistical Methods
All analyses were conducted using R statistical software (version 3.4.2; http://www.R- project.org). Normality of all response variables (burial duration, brood size, mean offspring size, sex ratio, and mean movement activity) were tested through Shapiro-Wilk tests. Burial duration, brood size, offspring sex ratio, and mean movement activity were non-normal. Burial duration and brood size were compared among treatments with generalized linear models. The effect of thermal treatment on burial duration was tested with a Poisson distribution and natural log link function. Because of a high dispersion index for brood size, the effect of thermal treatment on brood size was tested with a quasi-Poisson distribution and the natural log link function. The effect of thermal treatment on offspring sex ratio was tested using a Mann-
39 Whitney U test. To test the effect of temperature on breeding success, the proportion of breedings that produced larvae within each treatment was compared with a Pearson’s chi-squared analysis. Within temperature treatments, all movement activity counts registered for each individual over the three-day collection period were averaged. Mean activity was compared across treatments within each generation using Mann-Whitney U tests. The mean individual offspring size was normally distributed so the effect of the thermal environment was tested using a student’s T-test.
Results
Rearing Behaviors
At a temperature of 27.5°C, F1 breeding pairs exhibited a longer burial duration than control breeding pairs exposed to a temperature of 26°C (X2 = 3.95, df = 1, p = 0.0469; Fig. 3).
However, in the F2 generation burial duration did not differ between breeding pairs exposed to temperatures of 26.5°C and control 26°C (X2 = 0.698, df = 1, p = 0.4034; Fig. 3). This pattern
2 was the same in the F3 generation between exposures of 27°C and control 26°C (X = 0.0773, df
= 1, p = 0.7811; Fig. 3). Likewise, at 27°C, for F3 beetles whose parents (F2 generation) were reared in elevated temperatures (26.5°C; Step treatment), burial duration did not differ from F3 beetles whose parents (F2 generation) were not exposed to elevated temperatures (26°C; Control)
(X2 = 2.331, df = 1, p = 0.1268; Fig. 4).
Reproductive Success
Of the 30 breeding pairs (F1) in the Rapid treatment (27.5°C), only one produced larvae
(3.3%), while in the control (26°C), 72.2% breeding pairs produced larvae (a common frequency of success in captive breedings), indicating a significant effect of temperature on percent
40 2 breeding success (X = 29.417, df = 1, p < 0.0001; Fig. 5). In the F2 generation there was no significant effect of temperature on breeding success – the Step (26.5°C) and Control (26°C) treatments had a similar proportion of breeding pairs that produced larvae (X2 = 7.0194e-31, df =
1, p = 1.000; Fig. 5). However, breeding success of the F3 breeding pairs was significantly influenced by temperature treatment regardless of parental rearing temperatures—the thermal environment of 27°C had significant adverse effects on breeding success (X2 = 14.839, df = 2, p
= 0.0006; Fig. 5).
Brood Characteristics
Due to the significantly high failure rate of breeding pairs in thermal treatments of 27°C
2 2 (F3; X = 14.839, df = 2, p = 0.0006) and 27.5°C (F1; X = 29.417, df = 1, p < 0.0001), brood characteristics were analyzed only for the F2 generation with temperature treatments of 26°C and
26.5°C. Between these temperature treatments there was no difference in the number of offspring per breeding (F = 1.1997, df = 1, p = 0.2778), mean individual offspring size (t = -0.003, df =
35.916, p = 0.9976), or offspring sex ratio (W = 165.5, p-value = 0.9026; Fig. 6).
Movement Activity
F2 beetles exposed to elevated temperatures (26.5°C) were more active than beetles exposed to control temperatures (26°C; W = 6257, p-value = 0.0165; Fig 7). The rearing environment of these F2 beetles had no effect on the activity of their offspring (F3) in elevated temperatures (26.5°C; W = 5797, p-value = 0.8021).
Discussion
Identifying organisms of conservation priority requires an understanding of their vulnerability to projected climatic trends (Williams et al. 2008, Chown et al. 2010, Hoffmann and Sgró 2011, Huey et al. 2012). Species with the capacity to exhibit plastic changes, within or
41 across generations, in response to environmental perturbations are thought to have an adaptive advantage (Przybylo et al. 2000, Price et al. 2003, Réale, Berteaux, et al. 2003, Réale, McAdam, et al. 2003, Gienapp et al. 2008). While our findings suggest that, of the measured parameters, burying beetles do not exhibit transgenerational plasticity across our temperature treatments, evidence for within-generation behavioral plasticity is evident. Parents exposed to elevated temperatures increase burial duration and activity levels. Further, we provide evidence that N. marginatus reaches a thermal limit in their reproductive output at temperatures as low as 27°C.
Temperature is thought to be an important parameter influencing the activity of burying beetles (Merrick and Smith 2004, Nisimura et al. 2005). In the current study, activity levels of N. marginatus were measured in sustained environmental temperatures of 26°C and 26.5°C. Our findings suggest that this half a degree difference has significance effects on burying beetle activity – levels of activity were higher at higher temperatures, regardless of the level of thermal exposure of their parents. While the physiological mechanisms are uncertain (Pörtner 2001,
Farrell 2009), locomotor activity in ectotherms is expected to increase with temperature, a pattern that continues until they surpass their thermal optima, where activity then declines (Van
Donk and De Wilde 1981, Morgan 1985, Gannon et al. 2014, Halsey et al. 2015). Our findings support this trend; however, to comprehensively assess the thermal limits of burying beetles, their activity levels should be assessed across a spectrum of temperatures. Nonetheless, in the current study, though indirectly measured through alternative parameters, the decrease in thermal performance is evident at temperatures exceeding 26.5°C.
In rearing temperatures of 26.5°C and 27°C, the time it took breeding pairs of N. marginatus to bury the mouse carcass did not differ from those exposed to the control rearing temperature of 26°C. Further, offspring whose parents were reared in elevated temperatures
42 buried their carcasses at a similar rate to those with naive parents. At temperatures of 27.5°C, however, burial duration was longer than in the control groups. This increase in handling time of the carrion resource indicates a reduction in the rate of activity as it relates to the burial behavior, a possible byproduct of the physiological constraints imposed by thermal extremes. Because of the value of the carrion resource to myriad necrophilous organisms (Devault et al. 2003, Barton et al. 2013), the successful and efficient burial of a suitable carcass is important to counter both decomposition and usurpation by competitors (Eggert and Müller 1997, Scott 1998, Trumbo and
Bloch 2002). Therefore, this increase in burial duration implies a competitive disadvantage for burying beetles in projected climatic temperatures.
In our thermal treatments of 27°C and 27.5°C, breeding success rate was as low as 13.3% and 3.7%, respectively, suggesting an upper thermal limit on the reproductive output of N. marginatus. Characterizing the thermal sensitivity of organisms requires an understanding of how temperature relates to their fitness (Williams et al. 2008, Huey et al. 2012). As reproductive success rate contributes directly to fitness, it is highly valuable in assessing a species thermal performance (Huey and Stevenson 1979). Because these findings alone do not illustrate the full thermal performance curve of N. marginatus, future studies should address both the upper and lower limits on reproductive output to accurately link their thermal sensitivity to climate change resiliency. Furthermore, assessing the mechanisms behind this suspended reproduction, such as reproductive characteristics including fertility, will refine our understanding of climate change impacts on reproduction (Jørgensen et al. 2006, Walsh et al. 2019). Nonetheless, these results allude to direct fitness consequences for burying beetles subject to temperature shifts expected within their range.
43 As also demonstrated in activity levels and burial duration, in response to the thermal conditions of this study, N. marginatus do not exhibit TGP in the brood characteristics examined here. Parental exposure to elevated thermal environments had no effect on brood size, individual offspring size, or offspring sex ratio. Therefore, for burying beetles, TGP may not be an effective buffering mechanism in the face of climate change. This finding, and the overall results of this study, indicate potentially detrimental consequences of environmental change on burying beetle fitness. However, while the projected temperature increase in this region of Oklahoma for the end of the 21st century could be as high as 3°C (Oklahoma Department of Wildlife Conservation
2016), the realistic rate of warming will not match that of our experimental warming rate.
Because rate of warming is an important mechanism of TGP (Donelson et al. 2016), a more realistic temperature treatment across more generations may elicit plastic changes in burying beetles.
Overall, we demonstrate that elevated environmental temperatures have direct consequences on the fitness and competitive interactions of N. marginatus. In instances where ectothermic animals are exposed to habitats matching that of their thermal limits, behavioral thermoregulation, such as the exploitation of microclimates in heterogeneous environments, will be an important means of avoiding lethal temperatures (Kearney et al. 2009, Sunday et al. 2014,
Duffy et al. 2015). Alternatively, phenological or geographical range shifts (Parmesan 2006), as well as shifting daily activity patterns, may serve as potential buffers against environmental warming. Future work should assess the capacity of N. marginatus to exhibit these behavioral shifts. Furthermore, if this species’ geographic range will be restricted to more northward habitats, conservation efforts should aim to protect the remaining suitable habitat left for this
44 species in northern latitudes. Lastly, efforts should be made to understand the thermal limits of the Nicrophorus genus as a whole as their ecologies are often interrelated (Keller et al. in prep).
45 Figures
Fig. 1. The experimental design of this study. Beginning with the F0 progeny, at each generation, approximately 30 breeding pairs will be allowed to reproduce where parameters including carcass burial duration and breeding success will be measured. The offspring of each generational rearing experiment will be quantified, measured for size and sexed. A subset of these offspring will subsequently be placed in the varying temperature treatments for the next generational rearing experiment, where the procedure will repeat.
46
Fig. 2. Trikenetics activity monitor set-up for measuring the movement activity of N.marginatus individuals. For every time an individual passes the photo-eye (a), its activity is recorded as one count. During trials, individuals are housed in (b) plastic tubes with a (c) food source (raw pork loin) and (d) a water source (cotton plugs inserted in tube end) ad libitum.
47
Fig. 3. The duration of mouse burial (in hours) for breedings pairs subject to (a) the
1.5°C warming treatment in the F1 generation (26 vs. 27.5°C); (b) the .5°C warming treatment in the F generation (26 vs. 26.5°C); and the 1°C warming 2 treatment in the F generation (26 vs. 27°C). At 27.5°C (F generation; b), breeding 3 1 pairs exhibited longer burial duration (X2 = 3.95, df = 1, p = 0.0469) than at the control temperature.
48
Fig. 4. The duration of mouse burial (in hours) at 27°C for breedings pairs whose parents were reared in 26°C and 26.5°C. Parental rearing environment had no effect on the burial duration of their offspring in elevated temperatures (X2 = 2.331, df = 1, p = 0.1268).
49
Fig. 5. The percentage of breeding pairs that produced larvae for each temperature treatment. While there was no effect of a thermal environment of 26.5°C (n = 30; X2 = 7.0194e-31, df = 1, p = 1.000) on breeding success, in thermal environments of 27°C (n = 27; X2 = 14.839, df = 2, p = 0.0006) and 27.5°C (n = 27; X2 = 29.417, df = 1, p < 0.0001), breeding success was significantly reduced.
50
Fig. 6. The influence of thermal environment on (a) the number of offspring per breeding; (b) mean individual size; and (c) offspring sex ratio. There was no effect of a thermal environment of 26.5°C on these brood characteristics including brood size (F = 1.1997, df = 1, p = 0.2778), mean pronotum width (t = -0.003, df = 35.916, p = 0.9976), or offspring sex ratio (W = 165.5, p-value = 0.9026).
51
Fig. 7. The mean activity counts of burying beetles in thermal environments of 26°C and 26.5°C. Beetles exposed to increased temperatures exhibited higher movement activity than those exposed to the control temperature environment (W = 6257, p-value = 0.0165).
52 CONCLUSION
In this thesis work, I examined the temporal and spatial niche patterns of a speciose
Nicrophorine burying beetle community by empirically measuring the daily activity and approximating space use patterns of five co-occurring species. Additionally, I explored the response of N. marginatus, both within and across generations, to projected temperature change by monitoring rearing behaviors, movement activity, and brood characteristics with exposure to varying temperature regimes. I present results that represent spatio-temporal niche partitioning among sympatric burying beetles, as well as findings that indicate fitness costs in response to climate-induced temperature increases in the southern plains of North America.
Chapter 2 explored how sympatric burying beetles utilize space and time to partition the ephemeral resources necessary for reproduction. For the five beetle species co-occurring at the
Tallgrass Prairie Preserve, the overall interspecies space-use overlap was relatively low (below
30%). This pattern of low spatial overlap with all other species was most notable for N. marginatus. Interestingly, this species was found to be a temporal niche generalist, suggesting that space-use is the primary factor mediating competition among its congeners. For example, this interaction is evident between N. marginatus and N. tomentosus. While this species pair exhibited high temporal overlap, their spatial overlap was low. With the exception of one species pair, where spatial or temporal overlap is high, direct competition is mediated along an alternative niche dimension. For instance, N. pustulatus and N. tomentosus were highly overlapping in their space-use patterns but were temporally segregated. Likewise, N. americanus and N. orbicollis exhibited high temporal overlap, but are spatially segregated. Where this interplay of contrasting space-use and temporal activity patterns is lacking is between N. pustulatus and N. orbicollis. The spatial and temporal patterns documented here imply that these
53 species may be in direct competition. However, as N. pustulatus has been documented to exploit an alternative reproductive resource (Smith et al. 2007), these species may be ecologically separated through trophic niche partitioning.
The findings of this study are important in that they broaden our understanding of the three niche axes by which organisms may differ in their ecologies, and support the hypothesis that where competition for a limiting resource is intense, spatial and temporal niche patterns emerge. Furthermore, the findings of this study have direct implications for the conservation of the endangered American burying beetle (N. americanus Oliver). The methods by which the activity patterns were measured allowed for high temporal resolution thus unveiling an activity peak previously unknown for N. americanus (between 6:00 and 8:00am). We thereby recommend refining the trapping protocol for this species to occur after 8:00am. Furthermore, while direct competition among congeners is hypothesized as a factor in the decline of this species (Sikes and Raithel 2002), the findings of this study suggest that within the TGPP community, competition for the carrion resource is mediated by temporal and spatial niche segregation, and direct competition as an explanation for N. americanus decline is not supported.
Therefore, alternative decline hypotheses including habitat loss or increased pesticide exposure
(Sikes and Raithel 2002) should be explored.
In Chapter 3, I tested the influence of projected temperature trends on the reproductive biology and movement activity of N. marginatus and explored the capacity of this species to exhibit transgenerational plasticity as a buffer against the consequences of climate change.
Temperature was found to have direct influences on the movement activity, breeding behaviors, and reproductive success of N. marginatus. In higher temperatures, burying beetles exhibited increased activity, extended burial timing, and significantly reduced reproductive success rates.
54 Furthermore, there was no evidence that burying beetles exhibit transgenerational plasticity in reproductive behaviors, movement activity, or brood characteristics including offspring number and individual size, or offspring sex ratio. The findings of this study imply direct implications of temperature on the fitness of N. marginatus, and thus present a suite of questions about climate change resiliency in burying beetles.
Consistent with our findings, in ectotherms, the locomotor activity is expected to increase with temperature, until a thermal optima is reached where the activity will then decline (Van
Donk and De Wilde 1981, Morgan 1985, Gannon et al. 2014, Halsey et al. 2015). Future work on the movement activity of burying beetles as it relates to temperature should investigate at what temperature they reach their thermal optima. The findings of this study indicate that at soil temperatures as low as 27°C, reproductive success is alarmingly low, and at 27.5°C, burying beetles take longer to conceal their reproductive resource suggesting a competitive disadvantage.
Furthermore, of the measured parameters, there was no evidence for phenotypic plasticity as a response mediating these consequences. While the temperature treatments here represented middle to end of century warming, future work should assess whether slower rates of temperature change across more generations elicit behavioral modifications or plastic changes.
Furthermore, behavioral thermoregulation, including microhabitat exploitation or range shifts, should be considered as an important alternative for burying beetle persistence (Kearney et al.
2009, Sunday et al. 2014, Duffy et al. 2015).
Overall, the findings of these studies provide an understanding of the competitive interactions within a speciose burying beetle community and highlight negative fitness consequences associated with thermal variation in N. marginatus. There is an important interplay of space use and temporal activity facilitating the coexistence of this fascinating group of insects.
55 However, it is evident that in light of climate change, their persistence may be at stake. Efforts should be made to increase our understanding of the thermal capacity of the Nicrophorine genus as a whole.
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