Skip to main content
NCBI home page
Current Research in Insect Science logoLink to Current Research in Insect Science
. 2026 Mar 14;9:100124. doi: 10.1016/j.cris.2026.100124

Impacts of warmer temperatures on secondary seed dispersal by Phanaeus vindex dung beetles (Scarabaeinae)

Nathan Duerr 1,⁎, Kimberly S Sheldon 1
PMCID: PMC13050096  PMID: 41938908

Highlights

  • •

    The dung beetle Phanaeus vindex, a tunneling beetle, buried more seeds in the dung of food caches compared to brood balls.

  • •

    Experimental warming in mesocosms altered some but not all behaviors of this important secondary seed disperser.

  • •

    Impacts of warming on behavior of secondary seed dispersers can alter seed fate through shifts in plant-animal interactions.

Key words: Behavioral plasticity, Climate change, Endozoochory, Ecosystem functions, Seed burial

Abstract

Climate change impacts species interactions with cascading effects on ecosystem functions, including seed dispersal. Studies show that frugivore behaviors and associated seed dispersal are altered under climate change. However, little is known about how climate-induced behavioral shifts of non-frugivores, such as secondary seed dispersers, impact seed fate. Dung beetles are important secondary seed dispersers in many ecosystems because they bury seed-containing dung as either food caches for adult feeding or brood balls for reproduction. We utilized field manipulations with mini-greenhouses to investigate the effects of increased temperature on the seed dispersal behavior of a tunneling dung beetle species, Phanaeus vindex, in Tennessee, USA. Using beads as a proxy for seeds, we found that food caches contained more beads and were buried at shallower depths than brood balls. This suggests that food caches, which have largely been overlooked in previous studies, may play a key role in plant recruitment. Under warmer conditions in mini-greenhouses, we found that beetles buried food caches deeper than under control conditions, but food caches experienced similar temperatures regardless of treatment. For brood balls, we did not find a difference in burial depth or experienced temperatures between treatments. The greater burial depth of seeds in food caches under warmer conditions could adversely impact germination and emergence but could also buffer seeds in seed banks from the adverse effects of warmer surface temperatures. We conclude that climate change can alter secondary seed disperser behavior and thus plant-animal interactions, with ramifications for plant recruitment, community structure, and ecosystem functioning.

Introduction

Climate change is expected to alter species interactions and associated ecosystem functions, which are critical for maintaining healthy ecosystems (Åkesson et al., 2021; Hill et al., 2021; Peñuelas and Filella, 2001; Visser and Both, 2005). This is in part because the outcomes of species interactions are context-dependent and can change in response to different abiotic conditions (Chamberlain et al., 2014). As species respond differently to climate change, their unique shifts in behavior, phenotype, population size, and geographic range can alter species interactions. These alterations can in turn result in cryptic function loss, whereby the ecosystem functions provided by a species are lost without the loss of that species from the environment (McConkey and O’Farrill, 2015). Understanding how interspecific interactions will be shaped by species’ responses to climate change is thus essential for predicting future ecosystem functioning (Grünzweig et al., 2022; Strydom et al., 2021; Walther, 2010).

Seed dispersal by animals is a critical ecosystem function that could be disrupted by climate change, and these disruptions can either be exacerbated or mitigated by the behavioral shifts of dispersers (Harmon and Barton, 2013; McConkey and O’Farril, 2016; Sales et al., 2021). Over half of all plants rely on animals for seed dispersal, and these ecological interactions shape plant population dynamics, community structure, and recovery from disturbance (Beckman and Sullivan, 2023; Howe and Smallwood, 1982; Jordano, 2000; McConkey et al., 2012). For animals, behavioral shifts are often a first response to environmental change, but these shifts have consequences for seed dispersal (reviewed in McConkey and O’Farril, 2016). Currently, we have limited understanding of how seed dispersal behavior may be impacted by the warmer temperatures associated with climate change (Donoso et al., 2022; McConkey and O’Farrill, 2016). Previous research has primarily focused on changes in frugivore behavior in response to climate change, but the behavior of secondary seed dispersers remains an understudied yet important part of the overall seed dispersal process (Beckman and Sullivan, 2023; Nogales et al., 2024; Vander Wall et al., 2005).

Dung beetles are important secondary seed dispersers in many ecosystems (Nichols et al., 2008; Torabian et al., 2024), and their behaviors are sensitive to climate change (Kirkpatrick and Sheldon, 2022; Mamantov and Sheldon, 2021). Tunneling dung beetles locate a vertebrate dung source and then collect dung and bury it underground as dung deposits, which are either brood balls used for reproduction or food caches used for adult feeding. Because vertebrate dung often contains defecated seeds, these seeds can be moved away from the original dung source and secondarily dispersed underground within dung deposits. This secondary seed dispersal by dung beetles may facilitate escape from density-dependent mortality associated with seed predators and pathogens (Estrada and Coates-Estrada, 1991; Chambers and MacMahon, 1994). In addition, seed burial can provide a more suitable location for successful plant germination and growth (Chambers and MacMahon, 1994; Shepherd and Chapman, 1998). Despite a growing body of knowledge concerning the ecological importance of secondary seed dispersal by dung beetles, most research has been conducted in tropical regions with a conspicuous lack of studies in temperate North America (Andresen and Urrea-Galeano, 2022; Nichols et al., 2008).

Climate-induced changes in dung beetle behavior may alter secondary seed dispersal. Increased temperature can affect dung beetle behavior, with implications for the ecosystem services provided by dung burial, such as nutrient cycling and bioturbation (Gotcha et al., 2022; Holley and Andrew, 2018, 2020; Slade and Roslin, 2016). For example, several species of dung beetle have been shown to alter their breeding behavior in response to warmer temperatures, with brood balls buried deeper in warmer treatments (Kirkpatrick and Sheldon, 2022; Mamantov and Sheldon, 2021). Under future climate conditions, differences in burial depth of seeds and the temperatures they experience underground could greatly impact the survival of dispersed seeds (Benvenuti et al., 2001; Nyachiro et al., 2002; Toy and Willingham, 1966; Yang et al., 2003). This suggests that the altered nesting behavior of dung beetles could have implications for secondary seed dispersal, but this has not been investigated. In addition, literature on dung beetle food caches is sparse relative to brood balls (e.g., Hanski and Cambefort, 1991), and it is not known if or how warmer temperatures affect food caching behavior. The relative importance of each dung deposit type in overall secondary seed dispersal has also never been investigated.

In this study, we used field manipulations to investigate how warmer temperatures affect the secondary seed dispersal behavior of the dung beetle species Phanaeus vindex in Tennessee, USA. To measure changes in seed movement, we used glass beads as a proxy for seeds. Our study had three aims. First, we examined which dung deposit type (i.e., food caches or brood balls) contained more dispersed beads. Second, we measured burial depths of brood balls and food caches to understand how seed dispersal may be impacted by dung deposit type. Finally, we tested how warmer temperatures affect the amount of beads buried and the burial depth of both dung deposit types. Our study shows the implications of behavioral changes due to warmer temperatures for secondary seed dispersal, adding further insight into the ways that future climate conditions could impact plant-animal interactions and ecosystem functions.

Materials and methods

Study species

For our study, we used the tunneling dung beetle species, Phanaeus vindex Macleay, 1819, also known as the rainbow scarab, which is a medium-sized beetle (average female body length: 17.35 mm) native to the eastern USA (Wassmer and Armstrong, 2023). Phanaeus vindex invests in parental care by creating carefully constructed brood balls that are round and encased in a protective clay shell, while food caches are masses of dung loosely packed into tunnels. For this reason, P. vindex food caches appear superficially distinct from brood balls (Price and May 2009). The species can be readily bred in captivity, and individuals are reliably found near our study site.

Beetle collection

We collected P. vindex beetles on public grassland in Seven Islands State Park in Kodak, TN (35°57′10.9° N, 83°41′15.9° W) between April and July 2023. We used pitfall traps baited with cow dung to collect the beetles. Following methods in Kirkpatrick and Sheldon (2022), we maintained male and female beetles in captive colonies until the females were fertilized and ready for field experiments.

Experimental trials

Between June and August 2023, we conducted ten experimental trials in an open field on pastureland in eastern Tennessee. For each trial, following methods in Kirkpatrick and Sheldon (2022), we arranged six 7-gallon buckets (50 cm height x 31 cm top diameter x 26 cm bottom diameter) spaced 1 m apart. We cut four holes (5 cm diameter) into the bottom of each bucket to allow rainwater to drain, and we placed wire mesh at the bottom of the bucket to prevent beetle escape. We buried the buckets and backfilled each bucket with soil from the field, compacting the soil as much as possible and making the soil in the bucket level with the soil in the surrounding field. The soil in each bucket was 44 cm deep, which left 6 cm of open space at the top of the bucket for cow dung. We placed four HOBO data loggers (model: UA-001–64, Onset, Bourne, MA) in each 7-gallon bucket at depths of 1, 15, 29, and 43 cm to record temperatures every 30 min for the duration of the trial.

To start a trial, we removed female beetles from colonies and recorded beetle mass before randomly assigning a female to an experimental bucket. We added a single female to each bucket because fertilized females can store seminal fluid and will independently create and bury food caches and brood balls. We then placed a mixture of dung and beads at the soil surface of each bucket. For the mixture, we used glass beads (Luckkila brand seed beads) of three sizes (2, 3, and 4 mm in diameter) as a proxy for seeds. We chose these bead sizes because they are representative of seed sizes that P. vindex may encounter locally in the dung of native mammals (e.g., seeds of Callicarpa americana ∼2 mm, Rhus typhina ∼3 mm, Sassafras albidium ∼4 mm) (Beeman and Pelton, 1980; Eagle and Pelton, 1983; TN Seed Herbarium, 2024). We weighed 2 g of beads for each bead size (total of 6 g of beads) to standardize across bead sizes and then mixed these beads into 50 g of cow dung before providing this mixture to the beetles. We then covered the top of each bucket with wire mesh and a wire grate to prevent beetles from escaping and to keep non-experimental animals from disturbing the dung. Half of the buckets were then covered with miniature greenhouses that, based on our data loggers, passively increased temperatures at the soil surface by 2.1 °C (Fig S1), which is consistent with a previous study that used these methods (Kirkpatrick and Sheldon 2022). The other half of the buckets did not have greenhouses and acted as controls. Each female was given a unique ID, and because we were limited by the number of female beetles we could catch, some beetles were trialed twice, once in a control bucket and once in a greenhouse bucket.

Every 3 days during the trial period, we removed the unused dung/bead mixture at the soil surface and provided a fresh quantity of dung/bead mixture. The beetles never removed the entirety of the dung/bead mixture before the next feeding period. After a 9-day trial period, we carefully dug through the buckets by hand and gathered dung deposits. We gave each dung deposit a unique ID and recorded burial depth. We then brought the dung deposits to the lab where we recorded deposit type (food cache or brood ball) by breaking them open to determine if there was an egg present (i.e., brood ball) or not (i.e., food cache). We then placed dung deposits in a drying oven at 60 °C for 24 h, after which we recorded the mass. To recover beads from dung deposits, we placed a dried deposit into a strainer under running water. For each dung deposit, we recorded the number and mass of recovered beads for each bead size. Not all seeds stay within the dung during burial, and thus some seeds can be found within tunnels but outside of dung deposits. However, given the size of the 7-gallon buckets needed to capture P. vindex burial behaviors, it was not feasible to sift through the entire soil column for beads at the field site, save the soil for later processing, or use new soil for each trial. Thus, we did not record dispersed beads found within the soil column. Though this limits our ability to examine the entirety of secondary seed dispersal, our study still allows us to compare how secondary seed dispersal behaviors vary according to dung deposit type and thermal conditions.

In our study, burying behavior was restricted to within the diameter of the experimental buckets (top diameter: 31 cm, bottom diameter: 26 cm). Some dung beetle species create diagonal tunnels in nature, however, P. vindex tends to dig directly below dung sources. We placed dung in the center of the bucket, and thus, most tunnels we observed never reached the wall of the bucket. In addition, a study by Fincher (1973) found that P. vindex beetles in sandy clay loam pits (width, length, and height of 1.8 m) buried brood balls from 5–40 cm, with an average depth of 25 cm. Ritcher (1945) also states that P. vindex beetles buried brood balls at depths of 20.3–25.4 cm. These brood ball depths are comparable to what we observed in our study (see below), suggesting that buckets did not interfere with burial behavior.

Statistical analyses

We first examined which dung deposit type contained more beads and whether warming affected the amount of beads buried. To do this, we analyzed data from all dung deposits buried in both greenhouse and control buckets, including the dung deposits which did not contain beads. We used the bead mass per gram of buried dung in order to standardize across dung deposit type, and we then applied a square root transformation to these data to normalize the distribution. We fit a random intercept linear mixed-effects model (LME) in R (package lme4, R v. 4.5.1) with the response variable being the square root of bead mass per gram of dung in each dung deposit. We included the fixed effects of dung deposit type (brood ball or food cache), bucket type (greenhouse or control), and the interaction between dung deposit type and bucket type. We included the random effects of trial number and female identification (the unique code given to each female) since some beetles were trialed more than once and most beetles buried more than one dung deposit per trial. We compared weighted Akaike Information Criterion (wAIC) scores for each model against a null model that had the same random effect structure. For the final models, we provide the marginal R-squared value (R2m) (R package MuMIn) and the effect sizes of the fixed effects.

We next investigated burial depth of dung deposits and whether P. vindex females altered their burial behavior in response to warmer temperatures. For analysis, we fit a random intercept LME with the response variable being the natural logarithm of burial depth of dung deposits, the fixed effects of dung deposit type and bucket type, the interaction between dung deposit type and bucket type, and the random effects of trial number and female identification.

Lastly, we examined the temperatures experienced by bead-containing dung deposits and whether they varied based on dung deposit type and bucket type. To estimate the temperature experienced by each dung deposit, we followed methods in Kirkpatrick and Sheldon (2022) by using data from the four buried temperature loggers to fit a linear model of mean temperature recorded over the trial period as a function of burial depth (Fig S1). We used this relationship to then estimate the mean temperature experienced by each dung deposit for all ten trials. We then fit a LME model with the response variable of mean estimated temperature of the dung deposit, the fixed effects of dung deposit type, bucket type, and the interaction of dung deposit type and bucket type, and with the random effects of trial number and female identification.

Results

Over the course of ten trials, 35 Phanaeus vindex females created and buried 199 dung deposits, with 101 being brood balls (50 from greenhouse buckets, 51 from control buckets) and 98 being food caches (47 from greenhouse buckets, 51 from control buckets). Of these 199 dung deposits, 98 % (i.e., 195 dung deposits) contained beads. The dung deposits which did not contain any beads consisted of three brood balls and one food cache, all of which were from greenhouse buckets. Of the bead-containing dung deposits, 115 (59 %) included at least one bead of every size. Beetles were provided with an equal amount of each bead size by mass, and beetles buried all three bead sizes in similar amounts by mass (Fig S2).

We examined the amounts of beads contained in dung deposit types and whether warming affected the amounts of beads buried. We found a near-even split between bead-containing brood balls (n = 98) and food caches (n = 97). However, food caches buried by P. vindex contained more total bead mass per gram of dung than brood balls (Fig. 1a). On average, food caches also contained more beads of every size by number (2 mm: 11.10, 3 mm: 5.30, 4 mm: 2.00) compared to brood balls (2 mm: 9.75, 3 mm: 3.47, 4 mm: 0.95) (Fig S3). The model for buried bead mass per gram of dung in dung deposits included the fixed effects of dung deposit type and bucket type as well as their interaction (βfood cache = 0.09, βgreenhouse = −0.01, βfood cache x greenhouse = 0.03, wAIC = 1, R2m = 0.31). There were negligible changes in buried bead mass per gram of dung in response to warming or to the interaction between warming treatment and dung deposit type (Fig. 2).

Fig. 1.

Fig 1 dummy alt text

Open in a new tab

The combined mass of all sizes of buried beads (a) and burial depth (b) for brood balls and food caches. Boxplots include dung deposits from both control and greenhouse buckets. Boxplots show the median, 25th- and 75th-percentile (boxes), and the highest/lowest values not exceeding 1.5 inter-quartile ranges (error bars).

Fig. 2.

Fig 2 dummy alt text

Open in a new tab

The mass of buried beads per gram of dung in food caches (a) and brood balls (b) in control and greenhouse buckets. Boxplots show the median, 25th- and 75th-percentile (boxes), and the highest/lowest values not exceeding 1.5 inter-quartile ranges (error bars).

We next examined burial depth of dung deposits and whether P. vindex females altered their dung deposit burial behavior in response to warmer temperatures. The average temperature at 1 cm below the soil surface was warmer in the greenhouse (30.0 °C) compared to control (27.9 °C) buckets (Fig S1). The model for dung deposit burial depth included the fixed effects of dung deposit type and bucket type as well as their interaction (βfood cache = −0.46, βgreenhouse = 0.00, βfood cache x greenhouse = 0.19, wAIC = 1, R2m = 0.23). Food caches were buried at shallower depths than brood balls across bucket type (food cache depth: mean = 14.2 cm, standard deviation = 7.5 cm; brood ball depth: mean = 23.0 cm, standard deviation = 8.0 cm) (Fig. 1b). However, behavioral responses to warming varied by dung deposit type; food caches were buried deeper in greenhouse (15.7 ± 7.5 cm) compared to control (12.8 ± 7.3 cm) buckets (Fig. 3a), but brood balls were buried at similar depths in greenhouse (23.3 ± 7.7 cm) compared to control (22.6 ± 8.2) buckets (Fig. 3a, b).

Fig. 3.

Fig 3 dummy alt text

Open in a new tab

The burial depth of food caches (a) and brood balls (b) and estimated temperatures experienced by food caches (c) and brood balls (d) in control and greenhouse buckets. Boxplots show the median, 25th- and 75th-percentile (boxes), and the highest/lowest values not exceeding 1.5 inter-quartile ranges (error bars).

Based on temperatures recorded by the buried data loggers, we found no differences in the mean estimated temperatures experienced by food caches or brood balls in the greenhouse and control buckets (food cache mean temperatures: greenhouse = 27.3 °C, control = 27.4 °C; brood ball mean temperatures: greenhouse = 26.6 °C, control = 26.8 °C) (Fig. 3c, d). The model for dung deposit temperature included the fixed effects of dung deposit type and bucket type as well as their interaction (βfood cache = 0.34, βgreenhouse = −0.24, βfood cache x greenhouse = 0.27, wAIC = 0.75, R2m = 0.02).

Discussion

Our overarching goal was to investigate how warmer temperatures affect the secondary seed dispersal behavior of Phanaeus vindex dung beetles. To address this, we compared food caching and brood ball burial behaviors in the context of secondary seed dispersal and examined how warmer temperatures affect seed burial in these dung deposits. Using glass beads as a proxy for seeds, we found that nearly all dung deposits from P. vindex contained beads. In addition, food caches contained more beads and were buried at shallower depths than brood balls. Under the warmer conditions in greenhouse buckets, P. vindex placed food caches deeper than in control buckets, but the average temperatures that food caches experienced underground were similar in both bucket types. In contrast, brood balls were placed at similar depths in both greenhouse and control buckets, but the temperatures that these brood balls experienced underground were also similar across bucket types.

Food caching behaviors of dung beetles likely have greater benefits for plant recruitment than nidification behaviors. Seeds of many plant species experience optimal conditions for germination and emergence at soil depths of 1–5 cm, suboptimal but viable conditions at depths of 5–10 cm, and non-viability at depths greater than 10 cm (Benvenuti et al., 2001; Burmeier et al., 2010; Guo et al., 2010; Limón and Peco, 2016; Rokich et al., 2000). In P. vindex, one-third-of food caches containing beads were placed within viable depths for seeds (i.e., 10 cm from the soil surface), but all brood balls were placed at non-viable depths (i.e., deeper than 10 cm from the soil surface) (Fig S4). However, tunneling by dung beetles can move buried seeds to shallower depths (Andresen and Urrea-Galeano, 2022) and result in more permeable soil that could allow seedlings to push through the soil column and emerge from greater depths (Bang et al., 2005). Some locally occurring plants may even benefit from deep burial, such as the parasitic Conopholis americana, which requires contact with the roots of a host tree for germination (Baird and Riopel, 1986). In addition, seed survival in brood balls could be adversely affected by the beetle larvae, which have chewing mouthparts that could damage seeds, as well as by the protective clay shell constructed around brood balls that may prevent germination (Hata and Edmonds, 1983). The greater number and variety of seeds likely to emerge from the shallower placement of food caches compared with brood balls suggest that food caches may provide greater benefits for plant recruitment than brood balls.

Due to the behavior of adult beetles, some dung deposits contain more seeds than others. During food caching, adults move dung underground for later consumption (Hanski and Cambefort, 1991), but they can return to the surface to gather more food if needed (Price and May 2009). In contrast, dung provided by the adults in the brood ball is the only food source for developing larvae. During brood ball creation, adults expend energy filtering out large dung particles, reducing the C/N ratio of the dung and enhancing nutritional content for the offspring (Andresen and Feer, 2005; Byrne et al., 2013; Holter and Scholtz, 2007). These behaviors that maximize nutrition for offspring also result in seed removal from the brood ball, which may explain why food caches contained more beads than brood balls. However, higher seed density in food caches could also result in higher density-dependent mortality of seeds. Future studies examining seed germination and plant establishment in relation to both food caches and brood balls would be required to determine which dung deposit type is most beneficial for plant recruitment.

Behavioral plasticity of dung beetle food caching behavior compensates for warmer surface temperatures, protecting seeds against the adverse effects of heat associated with climate change. Warmer temperatures can decrease seed viability and increase germination speed (Luna et al., 2019), potentially leading to phenological mismatches in mutualistic interactions (Renner and Zohner, 2018). With hotter temperatures at the soil surface, P. vindex buried food caches deeper, effectively buffering any associated seeds from warming. However, despite brood balls being buried at similar depths in both control and greenhouse buckets, the temperatures experienced by brood balls were also similar across bucket type. Therefore, the relatively deep burial depth was sufficient to effectively buffer brood balls, and the associated seeds and larvae, from warmer surface temperatures.

Greater burial depth of seeds may reduce seedling emergence in the short term but could increase the long-term viability of seeds in seed banks. Temperature can be a crucial factor for the loss of seed dormancy, and as global temperatures continue to rise, seeds may experience increased mortality due to germination at inopportune times (reviewed in Ooi, 2012). However, greater burial depth buffers seeds against warmer surface temperatures and increases the long-term ability of seeds to survive in seed banks (Dwyer and Erickson, 2016; Mašková and Poschlod, 2022). Currently, we know little about fitness tradeoffs for plants associated with seed burial depth under increased temperatures. Future studies are needed to investigate how observed changes in the burial depth of seeds affect dormancy, germination, and emergence in order to understand the impacts of altered species interactions under warmer conditions.

Despite secondary seed dispersal being recognized as a vital link in the recruitment stage of plants, much work remains to be done in order to understand the complex species interactions involved and how they will be impacted by climate change (Beckman and Sullivan, 2023; Forget and Wenny, 2005; Nogales et al., 2024; Vander Wall et al., 2005). Warmer temperatures are impacting ecosystems worldwide, with some ecosystem functions being affected in unforeseen and cryptic ways (McConkey and O’Farrill, 2016, 2015). Though future climate change scenarios may differ from the effects of our greenhouses, and dung beetles may behave differently under less controlled environments, our results show beetles respond to temperature changes by adjusting certain burial behaviors. Our results thus illustrate that climate change alters plant-animal interactions, which has ramifications for ecosystem functioning, plant recruitment, and community structure in a rapidly changing world.

Declarations

Funding

This study was funded by the US National Science Foundation (grant no 2046368) and the University of Tennessee Herbarium Breedlove, Dennis fund.

Ethical approval

Not applicable.

Consent to participate

Not applicable.

Consent for publication

Not applicable.

Availability of data and material

Data will be made available from the Dryad Digital Repository upon publication and will be found under DOI: 10.5061/dryad.n02v6wx7s.

Code availability

All code used in this analysis is available publicly in R packages.

Author contributions

ND and KSS conceived of the study, designed methodology, and obtained funding. ND collected and analyzed data and wrote the manuscript. Both authors contributed critically to the drafts and gave final approval for publication.

Declaration of competing interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.

Acknowledgements

We thank Drs. Susan Riechert and Mac Post for allowing us to conduct research on their property, and Zan Killeffer and Ian Lauderback for assistance in the field. We are grateful to Dr. Charlie Kwit for fruitful discussions about seeds in Tennessee.

Footnotes

Supplementary material associated with this article can be found, in the online version, at doi:10.1016/j.cris.2026.100124.

Contributor Information

Nathan Duerr, Email: nathanlduerr@gmail.com.

Kimberly S. Sheldon, Email: ksheldon@utk.edu.

Appendix. Supplementary materials

mmc1.docx (403.7KB, docx)

References

  1. Åkesson A., Curtsdotter A., Eklöf A., Ebenman B., Norberg J., Barabás G. The importance of species interactions in eco-evolutionary community dynamics under climate change. Nat. Commun. 2021;12(1):4759. doi: 10.1038/s41467-021-24977-x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Andresen E., Feer F. In: Seed Fate: Predation, Dispersal and Seedling Establishment. Forget P.M., Lambert J.E., Hulme P.E., Vander Wall S.B., editors. CABI Publishing; UK: 2005. The role of dung beetles as secondary seed dispersers and their effect on plant regeneration in tropical rainforests; pp. 331–349. [DOI] [Google Scholar]
  3. Andresen E., Urrea-Galeano L.A. Effects of dung beetle activity on tropical forest plants. Front. Ecol. Evol. 2022;10 doi: 10.3389/fevo.2022.979676. [DOI] [Google Scholar]
  4. Baird WmV, Riopel J.L. Life history studies of Conopholis americana (Orobanchaceae) Am. Midl. Nat. 1986;116:140. doi: 10.2307/2425946. [DOI] [Google Scholar]
  5. Bang H.S., Lee J.-H., Kwon O.S., Na Y.E., Jang Y.S., Kim W.H. Effects of paracoprid dung beetles (Coleoptera: Scarabaeidae) on the growth of pasture herbage and on the underlying soil. Appl. Soil. Ecol. 2005;29:165–171. doi: 10.1016/j.apsoil.2004.11.001. [DOI] [Google Scholar]
  6. Beckman N.G., Sullivan L.L. The causes and consequences of seed dispersal. Annu Rev. Ecol. Evol. Syst. 2023;54(1):403–427. [Google Scholar]
  7. Beeman L.E., Pelton M.R. Seasonal foods and feeding ecology of black bears in the Smoky Mountains. Bears Their Biol. Manag. 1980;4:141. doi: 10.2307/3872858. [DOI] [Google Scholar]
  8. Benvenuti S., Macchia M., Miele S. Quantitative analysis of emergence of seedlings from buried weed seeds with increasing soil depth. Weed. Sci. 2001;49:528–535. doi: 10.1614/0043-1745(2001)049[0528:QAOEOS]2.0.CO;2. [DOI] [Google Scholar]
  9. Burmeier S., Donath T.W., Otte A., Eckstein R.L. Rapid burial has differential effects on germination and emergence of small-and large-seeded herbaceous plant species. Seed. Sci. Res. 2010;20(3):189–200. [Google Scholar]
  10. Byrne M.J., Watkins B., Bouwer G. Do dung beetle larvae need microbial symbionts from their parents to feed on dung? Ecol. Entomol. 2013;38:250–257. doi: 10.1111/een.12011. [DOI] [Google Scholar]
  11. Chamberlain S.A., Bronstein J.L., Rudgers J.A. How context dependent are species interactions? Ecol. Lett. 2014;17:881–890. doi: 10.1111/ele.12279. [DOI] [PubMed] [Google Scholar]
  12. Chambers J.C., MacMahon J.A. A day in the life of a seed: movements and fates of seeds and their implications for natural and managed systems. Annu. Rev. Ecol. Syst. 1994:263–292. [Google Scholar]
  13. Donoso I., Fricke E.C., Hervías-Parejo S., Rogers H.S., Traveset A. Drivers of ecological and evolutionary disruptions in the seed dispersal process: research trends and biases. Front. Ecol. Evol. 2022;10 doi: 10.3389/fevo.2022.794481. [DOI] [Google Scholar]
  14. Dwyer J.M., Erickson T.E. Warmer seed environments increase germination fractions in Australian winter annual plant species. Ecosphere. 2016;7 doi: 10.1002/ecs2.1497. [DOI] [Google Scholar]
  15. Eagle T.C., Pelton M.R. Seasonal nutrition of black bears in the Great Smoky Mountains National Park. Bears Their Biol. Manag. 1983;5:94. doi: 10.2307/3872524. [DOI] [Google Scholar]
  16. Estrada A., Coates-Estrada R. Howler monkeys (Alouatta palliata), dung beetles (Scarabaeidae) and seed dispersal: ecological interactions in the tropical rain forest of Los Tuxtlas, Mexico. J. Trop. Ecol. 1991;7(4):459–474. [Google Scholar]
  17. Fincher G.T. Nidification and reproduction of Phanaeus spp. in three textural classes of soil (Coleoptera: Scarabaeidae) Coleopt. Bull. 1973:33–37. [Google Scholar]
  18. Forget P.M., Wenny D. In: Seed fate: predation, Dispersal and Seedling Establishment. Forget P.M., Lambert J.E., Hulme P.E., Vander Wall S.B., editors. CABI Publishing; UK: 2005. How to elucidate seed fate? A review of methods used to study seed removal and secondary seed dispersal; pp. 379–393. [DOI] [Google Scholar]
  19. Gotcha N., Cuthbert R.N., Machekano H., Nyamukondiwa C. Density-dependent ecosystem service delivery under shifting temperatures by dung beetles. Sci. Total. Environ. 2022;807 doi: 10.1016/j.scitotenv.2021.150575. [DOI] [PubMed] [Google Scholar]
  20. Grünzweig J.M., De Boeck H.J., Rey A., Santos M.J., Adam O., Bahn M., Belnap J., Deckmyn G., Dekker C.S., Flores O., Gliksman D., Helman D., Hultine K.R., Liu L., Meron E., Michael Y., Sheffer E., Throop H.L., Tzuk O., Yakir D. Dryland mechanisms could widely control ecosystem functioning in a drier and warmer world. Nat. Ecol. Evol. 2022;6(8):1064–1076. doi: 10.1038/s41559-022-01779-y. [DOI] [PubMed] [Google Scholar]
  21. Guo C., Wang Z., Lu J. Seed germination and seedling development of Prunus armeniaca under different burial depths in soil. J. For. Res. 2010;21:492–496. doi: 10.1007/s11676-010-0104-1. [DOI] [Google Scholar]
  22. Hanski I., Cambefort Y. In: Dung Beetle Ecology. Hanski I., Cambefort Y., editors. Princeton University Press; Princeton, New Jersey: 1991. Competition in dung beetles; pp. 305–329. [Google Scholar]
  23. Harmon J.P., Barton B.T. On their best behavior: how animal behavior can help determine the combined effects of species interactions and climate change. Ann. NY Acad. Sci. 2013;1297(1):139–147. doi: 10.1111/nyas.12192. [DOI] [PubMed] [Google Scholar]
  24. Hata K., Edmonds W.D. Structure and function of the mandibles of adult dung beetles (Coleoptera: Scarabaeidae) Int. J. Insect Morphol. Embryol. 1983;12(1):1–12. [Google Scholar]
  25. Hill G.M., Kawahara A.Y., Daniels J.C., Bateman C.C., Scheffers B.R. Climate change effects on animal ecology: butterflies and moths as a case study. Biol. Rev. 2021;96(5):2113–2126. doi: 10.1111/brv.12746. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Holley J.M., Andrew N.R. Warming effects on dung beetle ecosystem services: brood production and dung burial by a tunnelling dung beetle, onthophagus taurus (Coleoptera: Scarabaeidae), is reduced by experimental warming. Aust. Entomol. 2020;59(2):353–367. [Google Scholar]
  27. Holley J.M., Andrew N.R. Experimental warming disrupts reproduction and dung burial by a ball-rolling dung beetle. Ecol. Entomol. 2018;44(2):206–216. [Google Scholar]
  28. Holter P., Scholtz H. What do dung beetles eat? Ecol. Entomol. 2007;32:690–697. doi: 10.1111/j.1365-2311.2007.00915.x. [DOI] [Google Scholar]
  29. Howe H.F., Smallwood J. Ecology of seed dispersal. Annu Rev. Ecol. Syst. 1982;13:201–228. doi: 10.1146/annurev.es.13.110182.001221. [DOI] [Google Scholar]
  30. Jordano P. In: Seeds: the Ecology of Regeneration in Plant Communities. 2nd edition. Fenner M., editor. CABI Publishing; Wallingford, UK: 2000. Fruits and frugivory; pp. 125–166. [Google Scholar]
  31. Kirkpatrick W., Sheldon K.S. Experimental increases in temperature mean and variance alter reproductive behaviours in the dung beetle phanaeus vindex. Biol. Lett. 2022;18 doi: 10.1098/rsbl.2022.0109. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Limón Á., Peco B. Germination and emergence of annual species and burial depth: implications for restoration ecology. Acta Oecologica. 2016;71:8–13. doi: 10.1016/j.actao.2016.01.001. [DOI] [Google Scholar]
  33. Luna B., Chamorro D., Pérez B. Effect of heat on seed germination and viability in species of Cistaceae. Plant Ecol. Divers. 2019;12:151–158. doi: 10.1080/17550874.2019.1610916. [DOI] [Google Scholar]
  34. Macleay W.S. Horae Entomologicae: Or, Essays on the Annulose Animals. Vol. 1. S. Bagster; 1819. [Google Scholar]
  35. Mamantov M.A., Sheldon K.S. Behavioural responses to warming differentially impact survival in introduced and native dung beetles. J. Anim. Ecol. 2021;90:273–281. doi: 10.1111/1365-2656.13366. [DOI] [PubMed] [Google Scholar]
  36. Mašková T., Poschlod P. Soil seed bank persistence across time and burial depth in calcareous grassland habitats. Front. Plant Sci. 2022;12 doi: 10.3389/fpls.2021.790867. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. McConkey K.R., Prasad S., Corlett R.T., Campos-Arceiz A., Brodie J.F., Rogers H., Santamaria L. Seed dispersal in changing landscapes. Biol. Conserv. 2012;146:1–13. doi: 10.1016/j.biocon.2011.09.018. [DOI] [Google Scholar]
  38. McConkey K.R., O’Farrill G. Cryptic function loss in animal populations. Trends. Ecol. Evol. 2015;30:182–189. doi: 10.1016/j.tree.2015.01.006. [DOI] [PubMed] [Google Scholar]
  39. McConkey K.R., O’Farrill G. Loss of seed dispersal before the loss of seed dispersers. Biol. Conserv. 2016;201:38–49. doi: 10.1016/j.biocon.2016.06.024. [DOI] [Google Scholar]
  40. Nichols E., Spector S., Louzada J., Larsen T., Amezquita S., Favila M.E. Ecological functions and ecosystem services provided by scarabaeinae dung beetles. Biol. Conserv. 2008;141:1461–1474. doi: 10.1016/j.biocon.2008.04.011. [DOI] [Google Scholar]
  41. Nogales M., McConkey K.R., Carlo T.A., Wotton D.M., Bellingham P.J., Traveset A., GonzálezCastro A., Heleno R., Watanabe K., Ando H., Rogers H., Heinen J.H., Drake D.R. A review on the State of the art in frugivory and seed dispersal on islands and the implications of global change. Bot. Rev. 2024;90(2):160–185. [Google Scholar]
  42. Nyachiro J.M., Clarke F.R., DePauw R.M., Knox R.E., Armstrong K.C. Temperature effects on seed germination and expression of seed dormancy in wheat. Euphytica. 2002;126:123–127. doi: 10.1023/A:1019694800066. [DOI] [Google Scholar]
  43. Ooi M.K.J. Seed bank persistence and climate change. Seed. Sci. Res. 2012;22:S53–S60. doi: 10.1017/S0960258511000407. [DOI] [Google Scholar]
  44. Peñuelas J., Filella I. Responses to a warming world. Science. 2001;294:793–795. doi: 10.1126/science.1066860. [DOI] [PubMed] [Google Scholar]
  45. Price D.L., May M.L. Behavioral ecology of Phanaeus dung beetles (Coleoptera: Scarabaeidae): review and new observations. Acta Zool. Mex. NS. 2009;25 doi: 10.21829/azm.2009.251621. [DOI] [Google Scholar]
  46. Renner S.S., Zohner C.M. Climate change and phenological mismatch in trophic interactions among plants, insects, and vertebrates. Annu Rev. Ecol. Evol. Syst. 2018;49:165–182. [Google Scholar]
  47. Ritcher P.O. Coprinae of eastern North America with descriptions of larvae and keys to genera and species (Coleoptera: scarabaeidae) Ky Agr. Expt. Sta. Bull. 1945;477:1–23. [Google Scholar]
  48. Rokich D.P., Dixon K.W., Sivasithamparam K., Meney K.A. Topsoil handling and storage effects on woodland restoration in Western Australia. Restor. Ecol. 2000;8:196–208. doi: 10.1046/j.1526-100x.2000.80027.x. [DOI] [Google Scholar]
  49. Sales L.P., Kissling W.D., Galetti M., Naimi B., Pires M.M. Climate change reshapes the eco-evolutionary dynamics of a Neotropical seed dispersal system. Glob. Ecol. Biogeogr. 2021;30(5):1129–1138. [Google Scholar]
  50. Shepherd V.E., Chapman C.A. Dung beetles as secondary seed dispersers: impact on seed predation and germination. J. Trop. Ecol. 1998;14(2):199–215. [Google Scholar]
  51. Slade E.M., Roslin T. Dung beetle species interactions and multifunctionality are affected by an experimentally warmed climate. Oikos. 2016;125(11):1607–1616. [Google Scholar]
  52. Strydom T., Catchen M.D., Banville F., Caron D., Dansereau G., Desjardins-Proulx P., Forero-Muñoz N.R., Higino G., Mercier B., Gonzalez A., Gravel D., Poisot T. A roadmap towards predicting species interaction networks (across space and time) Philos. Trans. R. Soc. B. 2021;376(1837) doi: 10.1098/rstb.2021.0063. [DOI] [PMC free article] [PubMed] [Google Scholar]
  53. TN Seed Herbarium, 2024. University of Tennessee Herbarium (TENN).
  54. Toy S.J., Willingham B.C. Effect of temperature on seed germination of ten species and varieties of Limnanthes. Econ. Bot. 1966;20:71–75. doi: 10.1007/BF02861928. [DOI] [Google Scholar]
  55. Torabian S., Leffler A.J., Perkins L. Importance of restoration of dung beetles in the maintenance of ecosystem services. Ecol. Solut. Evid. 2024;5(1) [Google Scholar]
  56. Vander Wall S.B., Kuhn K.M., Beck M.J. Seed removal, seed predation, and secondary seed dispersal. Ecology. 2005;86:801–806. doi: 10.1890/04-0847. [DOI] [Google Scholar]
  57. Visser M.E., Both C. Shifts in phenology due to global climate change: the need for a yardstick. Proc. R. Soc. B Biol. Sci. 2005;272:2561–2569. doi: 10.1098/rspb.2005.3356. [DOI] [PMC free article] [PubMed] [Google Scholar]
  58. Walther G.R. Community and ecosystem responses to recent climate change. Philos. Trans. R. Soc. B. Biol. Sci. 2010;365:2019–2024. doi: 10.1098/rstb.2010.0021. [DOI] [PMC free article] [PubMed] [Google Scholar]
  59. Wassmer T., Armstrong E. Population structure of Phanaeus vindex (Coleoptera: Scarabaeidae) in SE Michigan. J. Insect Sci. 2023;23(4):2. doi: 10.1093/jisesa/iead050. [DOI] [PMC free article] [PubMed] [Google Scholar]
  60. Yang X., Pritchard H.W., Nolasco H. In: Seed conservation: Turning Science Into Practice. Smith R.D., Dickie J.B., Linington S.H., Pritchard H.W., Probert R.J., editors. The Royal Botanical Gardens; Kew. Kew, UK: 2003. Effects of temperature on seed germination in six species of Mexican Cactaceae; pp. 575–588. [Google Scholar]

Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Supplementary Materials

mmc1.docx (403.7KB, docx)

Data Availability Statement

Data will be made available from the Dryad Digital Repository upon publication and will be found under DOI: 10.5061/dryad.n02v6wx7s.

Articles from Current Research in Insect Science are provided here courtesy of Elsevier

RESOURCES