J Insect Conserv (2008) 12:483–492 DOI 10.1007/s10841-007-9086-5
ORIGINAL PAPER
Factors affecting overwinter survival of the American burying beetle, Nicrophorus americanus (Coleoptera: Silphidae) Gary D. Schnell Æ Ana E. Hiott Æ J. Curtis Creighton Æ Victoria L. Smyth Æ April Komendat
Received: 21 January 2007 / Accepted: 12 April 2007 / Published online: 25 May 2007 Springer Science+Business Media B.V. 2007
Abstract The endangered American burying beetle (Nicrophorus americanus) is relatively abundant at Fort Chaffee Maneuver Training Center in northwestern Arkansas. There is a paucity of basic life-history information available, particularly with respect to factors affecting overwintering success. In a field experiment we: (1) captured beetles at Fort Chaffee; (2) bred them in captivity; (3) in the fall on Fort Chaffee placed offspring individually in well-ventilated, lidded 21.1-l buckets containing original soil plugs in grassland or woodland, either provisioned or not with a rat carcass as potential food; (4) overwintered the beetles; (5) checked in the spring to determine survival; and (6) released surviving beetles. Overall, 59.6% of 104 beetles survived the winter, with 77.1% and 44.6% survival in provisioned and nonprovisioned buckets, respectively. No differences were evident between habitats. Beetle age was an important survival predictor, with older beetles having a higher survival probability, but only if nonprovisioned. Gender and body size were not predictive of survival. Many surviving beetles were at or near the surface; depth averaged 6.0 cm, with some as deep as 20 cm. Our findings suggest that American burying beetles will have a higher probability of
G. D. Schnell (&) A. E. Hiott V. L. Smyth Sam Noble Oklahoma Museum of Natural History, University of Oklahoma, 2401 Chautauqua Avenue, Norman, OK 73072, USA e-mail:
[email protected] G. D. Schnell Department of Zoology, University of Oklahoma, Norman, OK 73019, USA J. C. Creighton A. Komendat Department of Biological Sciences, Purdue University Calumet, Hammond, IN 46323, USA
overwinter survival if carcasses are readily available as winter approaches. Keywords American burying beetle Endangered species Overwinter survival Nicrophorus americanus Provisioning
Introduction The American burying beetle (Nicrophorus americanus), once widespread over much of eastern North America, has disappeared from over 90% of its historic range and currently is restricted to the extreme eastern and western limits of that range (Lomolino et al. 1995). In 1989, the beetle was listed as an endangered species by the U.S. Fish and Wildlife Service (1991), which served as an impetus for researchers to increase our understanding of its breeding biology and ecology (e.g. Kozol et al. 1988; Ratcliffe and Jameson 1992; Creighton et al. 1993b; Lomolino et al. 1995; Lomolino and Creighton 1996; Holloway and Schnell 1997). Several proposals have been put forth to account for the decline of the species (Sikes and Raithel 2002). Explanations for the decline include habitat changes (loss, alteration, degradation), increased competition from vertebrates and congeners, and reduction in availability of optimal-sized carrion. However, none of the explanations to date are fully satisfying, and no single factor has been demonstrated to be causal. Two characteristics likely contributing to the species endangered status are its relatively large size and its specialized breeding behavior. The nocturnal American burying beetle is the largest North American member of the genus Nicrophorus. All members of the genus Nicrophorus breed on small vertebrate carcasses (size range 5–300 g; Trumbo 1992), a
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resource that is relatively rare and unpredictable in time and space (Hanski and Cambefort 1991; Eggert and Mu¨ller 1997). In contrast to smaller Nicrophorus species, the American burying beetle typically uses larger carcasses for reproduction (80–100 g preferred; Kozol et al. 1988; Trumbo 1992), making them dependent on a resource that is even more rare and unpredictable than that utilized by their smaller congeners. In addition, larger carcasses are harder to bury than smaller ones. Thus, the American burying beetle’s dependence on larger carcasses and its larger body size may, in part, explain why it has declined dramatically while other members of the genus remain relatively abundant and widespread. A central focus of research has been to understand the habitat requirements of the beetle. Anderson (1982) proposed the idea that American burying beetles were tied to old-growth forest, requiring the deeper and looser soils of such habitats. Lomolino and Creighton (1996) also suggested that, at a regional scale (i.e. across the forested, eastern one-third of Oklahoma), the American burying beetle is found predominantly in forests or woodlands with moderate undergrowth and deep soils. On a more local scale (Fort Chaffee, Arkansas, 29,000 ha; Camp Gruber, Oklahoma, 20,000 ha), the American burying beetle has been collected at baited pitfall traps in a range of habitats (Creighton et al. 1993b; Lomolino et al. 1995). In addition, individually marked beetles were observed moving between diverse habitat types (including grassland and woodland habitats, and upland and bottomland forests; Creighton and Schnell 1998). In Nebraska, recent records of the species are in grassland prairie, along forest edges, and in scrubland (Ratcliffe 1996; Bedick et al. 1999). Sikes and Raithel (2002) introduced the possibility that the species is actually a prairie specialist and that reforestation of much of its historic range has contributed to the decline of the species. Previous studies have focused on habitat associations and other aspects of the biology of American burying beetles during the summer breeding season, but many aspects of the ecology of the species during the nonbreeding season remain unstudied. For example, there is a paucity of basic information on the influence of habitat type, food availability, and body size on overwinter survival. Members of the genus Nicrophorus overwinter either in the larval or adult stage, depending on the species. Burying beetles that overwinter as larvae are dependent on where their parents locate a suitable carcass for reproduction. However, burying-beetle species that overwinter as adults have greater control over where they overwinter. Thus, habitat choice potentially could play an important role in overwinter survival for these species. Additionally, anecdotal field observations in eastern Oklahoma (J. C. Creighton, personal observation) suggest
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that American burying beetles may opportunistically overwinter in association with carrion, thus introducing the possibility that food might be an important parameter. We designed an experimental field study to assess the importance of habitat type and/or food availability on overwinter survival in the American burying beetle. Two basic questions were addressed: (1) Is there an effect of provisioning on winter survival? (2) Is there a difference in survival of American burying beetles overwintering in grasslands and woodlands? Secondarily, we were able to examine whether beetle size, sex, or age were related to the probability of overwinter survival. We also determined the depth in the soil where the overwintering beetles were located.
Methods Experimental protocol The American burying beetle is known to be relatively abundant on Fort Chaffee Maneuver Training Center in northwestern Arkansas (Schnell and Hiott 2005). The basic design of the study involved: (1) capturing American burying beetles on Fort Chaffee; (2) breeding pairs of these beetles in captivity; (3) using their offspring in the overwintering experiment at Fort Chaffee, where beetles were placed individually in large well-ventilated buckets with soil inside, either with or without carrion, and in grassland or woodland; (4) overwintering beetles in the buckets; (5) checking beetles in the spring to determine survival; and (6) releasing beetles that survived. Five trapping transects of baited pit-fall traps were set on 11 July 2005 as part of the annual American burying beetle survey at Fort Chaffee (Schnell and Hiott 2005). From the beetles captured at these sites, 18 mature pairs (one male and one female each; maturity determined by physical appearance) were selected and on 12 July 2005 shipped overnight to Purdue University Calumet, where these beetles served as brood stock. In total, they produced 177 offspring in the laboratory of which 120 were used in the overwinter field experiment. We established the following four field-study sites on Fort Chaffee, two in grassland habitat and two in woodland habitat: Grassland A (UTM Easting 388003, Northing 3902994); Grassland B (E 388485, N 3903475); Woodland A (E 387499, N 3901005); and Woodland B (E 389034, N 3902284). All were within 2.8 km of one another. On 15–16 July 2005 a grid of 30 21.1-l buckets (ca. 29.5 cm diameter at top, 25.5 cm diameter at bottom, and 35.5 cm height; i.e. slightly oversized 5-gal buckets) was established at each of the four sites. Buckets with lids were used to ensure that, after being introduced, the beetles
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could not escape by flying or digging out. Thus, if a beetle was missing, we would know that it had died versus having escaped from the bucket. In each bucket, holes were drilled in the sides and bottom to allow water to drain freely, and much of the top was replaced by heavy-duty screening so that there was ample air flow and ambient light inside the bucket. At each site, buckets were placed in a 6 · 5 array, with adjacent buckets 5 m apart. Each bucket was placed in a hole in the ground, with the upper rim 8 cm above the surface of the ground. When digging the hole, we removed the soil plug from the hole with as little disturbance as possible. The plug was then placed in the bucket intact to closely emulate natural conditions adjacent to the buckets. Soil gaps inside or outside of the buckets were carefully filled with soil to avoid air pockets. Bucket arrays were established about 3 months before stocking the experiment with American burying beetles to allow conditions in the buckets to equilibrate and, thus, closely resemble conditions outside the buckets. On 17 October 2005 the beetles used in the field experiment were shipped overnight from Purdue University Calumet to Fort Chaffee, each beetle being provided a small piece of liver as a food source. On 18 October each beetle was placed in an individual container after recording its age (from date it eclosed in the laboratory), sex, pronotum width (mm), and mass (g). Each beetle was provided five meal worms for food. American burying beetles were held in this manner in an air-conditioned room at 24C and under natural light conditions until 21 October because outside temperatures during 18–20 October reached over 32C on a daily basis. All beetles remained active and in excellent condition. On the morning of 21 October, a day when the high temperature dropped to 24C, 30 beetles were transported to each of the four sites and placed in individual buckets. Five meal worms were placed in each bucket, and oddnumbered buckets at each site were provisioned with a rat (Rattus norvegicus) carcass (mass ranged from 76 to 103 g). Lids were securely placed on each bucket. The buckets were checked three times during the experiment: 6 December 2005, 15 February 2006, and 3 April 2006. We removed the lids of each bucket and noted if American burying beetles were on the surface; the dirt inside the bucket was not disturbed. The experiment concluded with a final check on 24–28 April 2006, when temperatures reached 16C for three nights in a row—a temperature at which American burying beetles become active. During the course of the experiment, 16 of the buckets (five at grassland sites and 11 at woodland sites) were disturbed (lids detached, probably by people) and, thus, were removed from analyses. We replaced the lids during the experiment, but beetles were absent from these buckets
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at the end of the experiment, and it was not possible to determine whether they died and decomposed, or simply escaped from the buckets. Thus, results are based on findings for 104 buckets. Supplemental data gathered during course of experiment Soil samples were taken at four locations within each grid and analyzed for the percentage of silt, sand, and clay using a LaMotte Soil Texture Unit (Code 1067; LaMotte Company, Chestertown, MD), with preparation for testing following standard procedures (Foth 1970). Quantitative vegetation measures were taken at the same locations on 19 October 2005 following procedures taken from Tazik et al. (1992), Creighton et al. (1993a), Pogue and Schnell (1994), and Brower et al. (1998). Climatological data were extracted from monthly summaries made available through the National Climatic Data Center (Asheville, North Carolina) for Fort Smith Regional Airport. Initially and for each check of the sites we measured soil temperature and moisture inside and outside 10 buckets at each site with an Aquaterr digital meter (T-300; Aquaterr Instruments, Costa Mesa, CA) inserted in the soil to a depth of 15 cm. Statistical analyses Paired comparisons of soil temperature and moisture values inside and outside of the experimental buckets were made employing a two-way ANOVA without replication (Sokal and Rohlf 1995). A single-classification ANOVA was used to compare changes in mass of surviving beetles provisioned with a rat carcass and those that were not, as well as for comparisons between grassland and woodland sites of soil temperatures and moistures inside the buckets. Analysis of the survival results for the overall experiment was conducted on a three-way contingency table using a log-linear model (Sokal and Rohlf 1995), with the three factors being habitat, provisioning, and survival. The significance of a term in the overall log-linear model is tested by calculating the difference between G-values for models with and without the term. Testing for any particular effect (e.g. the interaction of factors A and B) depends on the other effects included in the particular log-linear model. As a result, several appropriate ways exist for evaluating the strength of a given effect. We used two tests—those involving marginal and partial associations—to determine the significance of an effect. These two estimates of importance and their associated G-values provide similar, although not necessarily identical statistical results. When tests for complete independence or the highest-order interaction (in our case the three-way interaction) are conducted, marginal and partial associations
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Characteristics of sites Soils of all sites had relatively little clay, with from about 35 to 75% silt and 25 to 60% sand. There was broad overlap in the composition of soils from grassland and woodland sites (Fig. 1). The grasslands were predominantly little bluestem (Schizachyrium scoparium), with other grasses and forbs present. The woodlands were typical Cross Timbers habitat (Ku¨chler 1964), with the dominant species being post-oak (Quercus stellata), blackjack oak (Q. marilandica), and red cedar (Juniperus virginiana). For vegetation structure and related physical attributes, grassland sites were very similar to one another, as were the two woodland sites. In square-meter sampling areas on the ground, grasslands had on average a higher percentage of woody plants (13.1 vs. 6.9%) and grasses (43.1 vs. 5.0%), while the woodland sites had more litter (43.8 vs. 20.0%) and dead wood (21.9 vs. 6.3%). On grassland and woodland sites, coverage by forbs (16.3 vs. 18.1%) and bare ground (1.3 vs. 3.8%) were about the same. The grasslands on average had a higher number of hits on the 1-m rod held 1 m above the ground (1.09 vs. 0.31). The
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Silt (%) 0 Grassland A Grassland B Woodland A Woodland B
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80
20
90
10
100
Clay (%) 0
0
10
20
30
40
50
60
70
80
90
100
Sand (%)
Fig. 1 Ternary plot showing percentages of silt, sand, and clay in four soil samples taken from each of the four grids. In some cases, soils were the same and, thus, symbols overlap. The labels silt, sand, and clay are at apices representing 100% of these components, respectively
grasslands were completely open, while the canopy was 82% closed in the woodlands. Not unexpectedly, the number of decimeter intervals with vegetation hits on the lower part of a vertical pole (0.0–2.5 m) were on average more frequent in the grassland (4.00 vs. 2.50), while the hits high (2.5–7.5 m) were more frequent in the woodland (3.88 vs. 0.00). There was no canopy in the grassland, while it extended to over 9 m in the woodland. As expected, the mean distance to the nearest tree was much less in the woodland than in the grassland (9.1 vs. 19.6 m). Air temperatures were highly variable, both daily and over the course of the 190-day experiment (Fig. 2). The maximum daily temperature was above freezing on all but two of those days, although on 66 days (34.7%) the minimum was at or below freezing. Temperatures fluctuated 35 30 25
Daily temperature (°C)
give identical numerical results. The three-way log-linear model was obtained using BIOMstat version 3.30q (Rohlf and Slice 1999). We employed a Williams correction (Sokal and Rohlf 1995), which has the effect of reducing the observed G-value slightly and provides a better approximation to the chi-square distribution with which values are compared. We also analyzed the relationship of survival to multiple factors using stepwise logistic regression (Hosmer and Lemeshow 2000; Pampel 2000). The dependent variable was whether the beetle was dead or alive (0 or 1) at the end of the experiment, with the following considered as potential independent predictor variables: (1) provisioning (whether or not a rat carcass was provided); (2) habitat (grassland or woodland); (3) age (age in days since emergence in laboratory); (4) sex (male or female); (5) pronotum width (in millimeters); and (6) mass of beetle at initiation of experiment (in grams). The significance level to include a variable was set at 0.05, as was the significance level to remove. The maximum number of steps was limited to 10. McFadden’s q2-statistic, which can vary from 0 to 1, was used to evaluate resulting models as a whole. It is a transformation of the likelihood-ratio statistics intended to mimic R2, with higher values indicating more substantiated results. Steinberg and Colla (2004) noted that q2-values tend to be lower than R2-values (0.20–0.40 have been considered to be very satisfactory) and that a low value does not necessarily indicated poor fit of the model. Calculations were completed using Systat 11 (Systat Software 2004).
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20 15 10 5 0 -5 Maximum Minimum
-10 -15 Oct
Nov
Dec
Jan
Feb
Mar
Apr
Date (2005-06)
Fig. 2 Maximum and minimum daily temperatures (C) during course of 190-day field experiment (21 October 2005–28 April 2006) based on records of the National Climatic Data Center for Fort Smith Regional Airport
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considerably within any 24-h period, with the average difference between the minimum and maximum being 14.3C. Temperatures in October, November, December, February, and March were relatively close to 30-year averages (Table 1). However, temperatures in January were unseasonably warm, being on average 5.39C above the long-term average. Temperatures dipped below freezing in each month from November through March, although in all months of the study, average temperatures were considerably above freezing (Table 1). For the first part of our experiment (October–December), precipitation was considerably less than normal (Table 2). This also was the case for February, while January, March, and April had precipitation values somewhat above 30-year averages. In general, soil temperatures inside and outside of the buckets were relatively similar (Table 3). Initially (19 October), the bucket temperatures averaged 0.11C less than found in the adjacent ground. On 6 December the temperatures also were slightly lower in the buckets, but inside–outside temperatures were not statistically different. During the two subsequent checks (15 February and 3 April), temperatures were slightly higher in the buckets than in the adjacent soil; for the final check (24 April), temperatures were virtually the same. Soil temperatures inside buckets were higher statistically in grasslands than in woodlands on 19 October, 6 December, and 3 April (differences of 2.55, 1.63, and 1.03C, respectively; all P < 0.01), but not so on 15 February or 24 April (P > 0.05). For all five check periods, soils in buckets were moister than soils adjacent to the buckets (Table 3), but soil moistures within buckets were not different between grassland and woodland sites (P > 0.05). While we had numerous holes drilled in the sides and bottoms of the buckets to facilitate drainage, the buckets consistently did hold moisture more readily than was the case in the adjoining soil. The effect of this increased moisture on the results of the experiment is unknown. However, the influence was essentially the same on all parts of the experiment.
Table 2 Precipitation (mm) for months during which study was conducted in 2005 and 2006 (based on records of the National Climatic Data Center for Fort Smith Regional Airport) Month
Total precipitation
Departure from normala
Greatest day
October
31.2
–68.8
30.2
November
21.1
–100.8
17.5
December January
9.9 78.5
–76.2 18.3
5.1 42.9
February
16.0
–49.8
8.9
March
134.9
34.8
38.1
April
135.4
36.1
55.1
a
Averaging period 1971–2000
Results During the final check in late April 2006, we recorded the depth in the soil at which 61 of the 62 surviving American burying beetles were found (Fig. 3). Beetles were buried in the soil from 0 to 20 cm, with a mean depth of 6.0 cm (SD 5.4 cm). Many of the beetles were at or just below the surface, but some were positioned at a considerable depth. No statistically significant differences in depth were found among the four sample sites, between grassland and woodland locations, or between provisioned and nonprovisioned buckets (ANOVAs; all P > 0.05). Furthermore, a two-way ANOVA did not find a significant difference in depth when considering habitat (grassland versus woodland) and provisioning (provisioned versus not provisioned) simultaneously (P > 0.05). Differences in survival between the two grassland sites and between the two woodland sites were not significant statistically (P > 0.05), so data from habitat replicates were combined. The overall results are summarized in Table 4, partitioning the data with respect to provisioning, habitat, and survival. Overall, 59.6% of the American burying beetles survived the winter, with survival of those provisioned with a rat carcass being 77.1% and those not provisioned being 44.6%.
Table 1 Temperature (C) characteristics for months during which study was conducted in 2005 and 2006 (based on records of the National Climatic Data Center for Fort Smith Regional Airport) Highest
Lowest
Average maximum
Average minimum
October
24.78
10.72
17.78
0.67
33.3
0.6
November
19.50
4.67
12.11
1.83
28.9
–6.1
December
11.50
–2.28
4.61
–0.39
24.4
–12.8
January
16.28
1.11
8.72
5.39
24.4
–7.8
February March
13.28 19.50
–0.94 6.06
6.17 12.78
–0.33 1.33
26.7 30.0
–7.8 –2.8
April
26.72
12.61
19.67
3.50
35.6
5.0
a
Average
Departure from normala
Month
Averaging period 1971–2000
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Table 3 Average ground temperature and moisture at depth of 15 cm both inside and outside of buckets at various times during field experiment Date
Average temperature differencea
Average temperature (C) Inside
Outside
19 Oct 2005
21.44
21.56
6 Dec 2005
6.89
6.89
Average moisture (%)
Average moisture differencea
Inside
Outside
–0.11*
69.3
37.5
31.8***
–0.06ns
71.2
50.0
21.2*** 18.1***
15 Feb 2006
8.89
7.83
0.94***
77.1
57.0
3 Apr 2006
19.22
19.11
0.11*
60.6
53.2
6.6**
24 Apr 2006
18.28
18.28
–0.06ns
75.5
58.3
15.5***
ns
, P > 0.05; *, P < 0.05; **, P < 0.01; ***, P < 0.001
a
Average difference between paired measurements (inside value-outside value)
0
1
2
3
0
1
2
3
4
5
6
7
8
9
10
4
5
6
7
8
9
10
0 2 4
D epth (cm)
6 8 10 12 14 16 18 20
Number of beetles Fig. 3 Depth in soil at which 61 surviving American burying beetles were found during the final check 24–28 April 2006 Table 4 Number (with percentage in parentheses) of American burying beetles alive or dead at end of experiment for the four sites, with indication as to habitat and whether beetles were provisioned with a rat carcass Provisioning and habitat With rat
Survival
Subtotal or total
Alive
Dead
37 (77.1)
11 (22.9)
48
Grassland
24 (85.7)
4 (14.3)
28
Woodland
13 (65.0)
7 (35.0)
20
Without rat
25 (44.6)
31 (55.4)
56
Grassland
12 (44.4)
15 (55.6)
27
Woodland Total
13 (44.8) 62 (59.6)
16 (55.2) 42 (40.4)
29 104
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The statistical findings based on the three-way contingency analysis using a log-linear model are provided in Table 5. First, considering the three factors simultaneously, we rejected statistically the hypothesis that there was complete independence of the factors (G = 15.19, P < 0.001). Second, we did not test for independence of habitat and provisioning, since the design determined the number in each habitat being provisioned; the values from the analysis simply reflect the fact that, because some buckets were eliminated during the course of the experiment, the final numbers being provisioned in each habitat type were not equal. Third, survival proportions were not different (P > 0.05) in grasslands and woodlands, when considered statistically by holding the effect of provisioning constant. Fourth, there was a statistically significant relationship between provisioning and survival, with those American burying beetles that were provided with rat carcasses having a substantially higher survival rate (P < 0.01 based on a partial association and P < 0.001 on a marginal association; Table 5). Survival was more than 30% higher when a rat carcass was available to the beetle. Finally, there was no evidence of a significant interaction of the three factors (G = 1.73, P > 0.05). The average mass loss for surviving American burying beetles that were provisioned was 0.092 g (8.80% of initial mass), while that for beetles that were not provisioned was 0.134 g (11.83% of initial mass). However, given the wide variance in mass change in both groups, neither the differences in change in mass or in the percentage change in mass are statistically different (P = 0.433 and 0.588, respectively). The stepwise logistic regression on the 104 buckets (contrasting the 62 where the American burying beetle survived with the 42 where the beetle died) resulted in the following equation: Y ¼ 1:351 þ 1:411X1 þ 0:046X3 ; where Y is the dependent variable (coded 0 if beetle was dead and 1 if beetle was alive at the end of the field
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Table 5 Summary of statistical evaluation of log-linear model for data on American burying beetles considering three factors—habitat, provisioning, and survival Hypothesis tested
df
G-valuea Partial association
Habitat · provisioning independence Habitat · survival independence
Marginal association
0.431b
1
1.314b
ns
1.900ns
1
1.005
Provisioning · survival independence
1
10.712**
Habitat · provisioning · survival interaction
1
1.726ns
Habitat · provisioning · survival independence
4
15.189***
11.607***
a Both partial and marginal associations are used to test independence and interactions. Results of tests for marginal and partial associations are equal when evaluating complete independence or the highest-order interaction. Statistical significance: ns, P > 0.05; **, P < 0.01; ***, P < 0.001 b
Not tested, since set by experimental design
experiment), X1 is provisioning (a 0 if no rat provided; 1 if rat provided; P = 0.002), and X3 is age of beetle (in days from emergence in laboratory; P = 0.022). McFadden’s q2 was 0.123. Habitat, sex, pronotum width, and initial mass were not predictive as to whether or not a beetle survived and, thus, did not enter the equation. As was found with the three-way log-linear model, the equation for the logistic regression indicates the importance that provisioning played in enhancing the survival probability of the beetle. In addition, age (which varied from 5 to 44 days) was a significant factor, with older individuals more readily surviving than younger beetles. The analysis was repeated, considering only the 56 buckets that were not provisioned with a rat carcass (thus, of course, the provisioning variable was not relevant). For this group the beetles in 25 survived and 31 did not. The resulting equation was: Y ¼ 1:857 þ 0:066X3 : For the beetles that were not provisioned with a rat, the only factor predictive of survival was the age of the beetle (P = 0.013), with older beetles having a higher probability of survival. The value for McFadden’s q2 was 0.091. Considering only those beetles that were not provided with a rat carcass, habitat, sex, pronotum width, and initial mass were not indicative of survival. The analysis was repeated a third time, considering only the 48 buckets that were provisioned with a rat carcass, for which 37 beetles survived and 11 died. For these beetles, none of the variables (habitat, age, sex, pronotum width, or initial mass) provided insight as to whether or not the beetle survived. Thus, the second and third logisticregression analyses suggest that only for beetles not provisioned was age a predictive factor with respect to survival; in this group the older beetles had a better chance of survival. Age was not a factor in survival when a rat carcass was provided.
Discussion A majority of the American burying beetles survived the winter, with 59.6% being alive in late April. The presence of carrion had a significant impact on American burying beetle overwinter survival (77.1% survived in provisioned buckets compared to 44.6% in buckets not provisioned). While no direct quantitative information is available on the extent to which American burying beetles normally overwinter in association with animal carcasses, our data show that there is a survival benefit for those that do. Anecdotal evidence indicates that American burying beetles overwinter with carrion at least on occasion. At a site in eastern Oklahoma, American burying beetles were observed in association with carcasses placed in the field in early October, well after the breeding season. Specifically, several beetles were found in small tunnels dug into the soil directly under rat carcasses (J. C. Creighton, personal observation). In fact, a number of the beetles in our experiment constructed the same type of tunnels into the soil under provided carcasses. Our experimental results indicate that one can enhance overwinter survival by provisioning American burying beetles with carrion. In our experiment, conducted in buckets with lids, carcasses were protected from usurpation by competitors, unlike in nature where carcasses likely would attract a variety of scavengers. However, by the time of our first check about half of the rats had been buried or mostly buried by the beetles, an action that in nature would result in the sequestering of carcasses from other scavengers. We suspect the burying occurred early in the experiment. We found no evidence of a difference in survival in grasslands and woodlands, irrespective of whether American burying beetles were provided with a rat carcass. While the beetles in our study were not able to choose the habitat in which to overwinter, the results suggest that gross habitat differences are probably of little consequence with respect to overwinter survival. These results are consistent
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with previous studies examining summer habitat preferences of the American burying beetle at local scales (i.e. Fort Chaffee). These studies demonstrated that American burying beetles have the broadest niche breadth of buryingbeetle species found in eastern Oklahoma and western Arkansas (Lomolino et al. 1995; Lomolino and Creighton 1996; Schnell and Hiott 2005) and are captured in baited pitfall traps set in a variety of habitats (Creighton et al. 1993b; Lomolino et al. 1995; Lomolino and Creighton 1996; Schnell and Hiott 2005). In addition, individually marked beetles readily move between habitats (including grassland and woodland habitats, and upland and bottomland forests; Creighton and Schnell 1998). While we found no differences in winter survival between grasslands and woodlands, this is not to say that habitat differences do not influence other aspects of the American burying beetle’s natural history. For example, Walker and Hoback (2007) noted that encroachment by red cedars affected American burying beetles, with more first-time captures in open habitat than in cedar-dominated habitat, but more recaptures in the latter. They suggested that in cedar-dominated areas American burying beetles are less likely to disperse. Given that grassland and woodland sites used in the study overlapped broadly in terms of soil characteristics, the potential effect of overwintering in different soils was not evaluated in our experiment. At the end of the experiment, surviving beetles were found anywhere from on the surface to a depth of 20 cm, with the average depth being 6.0 cm. These data suggest that soil depth may not be a serious constraint on overwinter survival in this part of the species’ range. However, further work is needed to clarify the possible importance of both soil type and depth. We found no evidence that body size or gender influenced survival. In contrast to our results, studies have demonstrated that body size is an important factor in survival of some insects. In the burying beetle Nicrophorus investigator, larger larvae were more likely to survive through the winter than smaller larvae (Smith 2002). In addition, several field tests of the size–fitness relationship in insects have demonstrated that being large increases adult survival (Visser 1994; West et al. 1996; Bennett and Hoffmann 1998; Ellers et al. 1998). In our experiment, the age of American burying beetles had a significant influence on overwinter survival. Specifically, we found that older beetles had a higher survival probability when overwintering without a carcass, but age was not a factor of importance if wintering was accomplished in association with carrion. There are at least two explanations for this surprising result. First, many of the younger beetles used in this experiment were not sexually mature, which occurs at about a month of age for the American burying beetle (Bedick et al. 1999). Sexual maturity may be an important parameter determining
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overwinter survival. However, this supposition does not fully explain why only young beetles overwintering without a carcass were affected. A more likely explanation is that younger beetles may not have had the opportunity to store sufficient fat reserves to survive through the winter without access to carrion. All beetles in the experiment initially were supplied with meal worms when placed in the field. However, carrion may be an important food source after eclosion. This conclusion underscores the importance of newly eclosed beetles having access to carrion prior to winter diapause. The lower survival of nonprovisioned young beetles also could be related to environmental factors that are particularly important in the southwestern portion of the range of the American burying beetle. Temperatures ranged widely (Fig. 1) from below freezing to very warm throughout much of the study (i.e. November–March), with the average temperature being below freezing only in December and February (Table 1). Thus, there often was pronounced warming and cooling, with significant fluctuations occurring weekly and in some cases even daily. Tolerance of low temperature per se at the latitude of Fort Chaffee probably would not be the most critical factor, given that ground temperatures seldom stay below freezing for long. Rather, the physiological challenge more likely involves cold tolerance and stress resistance of the American burying beetle and its response to repeated warming–cooling cycles, fast temperature changes, possibly numerous freeze–thaw transitions, and general climatic unpredictability (Sinclair et al. 2003). Fitness modeling suggests that winter survival with minimal energy expenditure in ectotherms is not only sensitive to the number of freezing days and low temperature stress, but also to the quantity of energy resources stored and the extent of environmental variation encountered (Voituron et al. 2002; Sinclair et al. 2003). While freezing itself can be a significant factor in mortality, it is known, for example, that in the fly Eurosta solidaginis higher than normal temperatures can lead to elevated metabolic rate in larvae, resulting in an actual decrease in survival, as potential energy reserves are depleted (Irwin and Lee 2000). While speculative, the effect could be the same in adult American burying beetles if, under similar circumstances, a food source is not readily available. The generality of our findings is limited to some extent by two factors—that the study was conducted in only one part of the American burying beetle’s range and that we only were able to conduct the experiment for a single season. Challenges to overwinter survival can vary substantially from region to region. As discussed above for Fort Chaffee, which is in the southern part of the beetle’s current range, stresses likely come from the variation in temperatures, with the chance that beetles periodically will become physiologically active at various points during the
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winter, thus significantly diminishing stored energy reserves. In more northerly areas, the challenges to overwinter survival include the extended period of cold, the lowness of the temperature, and the depth of the frost line in the soil. It would be of interest to know more about overwinter survival in more northerly areas. At Fort Chaffee, high intrayear and interyear variability in winter weather is typical. Temperatures during our study were about normal, except for January when it was unseasonably warm. Had we chosen a different year for our investigation the temperature regime could have been decidedly different. Nevertheless, the notable day-to-day and within-day temperature fluctuations experienced during our study are fully characteristic of the southern part of the American burying beetle’s range. Overall survival likely varies substantially from year to year and the survival rates during our study probably are higher than would be the case for winters with more extreme weather conditions. Given that Fort Chaffee often has some relatively long warm periods during the winter, we suspect that, if given the opportunity, American burying beetles will feed, thus responding to increased metabolism that is concomitant with higher temperatures, while at the same time replenishing reserves. Thus, those American burying beetles that were provisioned with a rat carcass had the opportunity to feed, possibly a number of times during the winter, which could well lead to an increased probability of survival. Furthermore, young beetles not provisioned under such circumstances would be particularly disadvantaged. The quality of energy resources stored and the extent of environmental variation encountered can be significant determiners of mortality (Sinclair et al. 2003). Moisture levels may have a substantial impact on overwinter survival. For a related species, Bedick et al. (2006) found in the summer that Nicrophorus marginatus was unable to survive low-humidity conditions for long without access to water. Under desiccating conditions, the beetles died after losing about 30% of their body mass, which sometimes occurred in as little as 8 h. In our study the somewhat elevated moisture levels encountered in the experimental buckets relative to those in surrounding soils (Table 3) probably had a positive effect on survival. Furthermore, we suspect that provisioning would result in an even greater enhancement in survival during drier winters. Our experiment allowed us to evaluate the use of 21.1-l buckets for field experiments with the endangered American burying beetle. The overall winter survival rate of 59.6% over the course of this experiment suggests that these containers were very appropriate for the field study we conducted. While we only checked the depths at which beetles were positioned at the end of the experiment, none of the beetles at that time were at or near the bottom of the containers; it appears that the buckets did not restrict the
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beetles from moving to appropriate depths in the soil. Soil temperatures in the buckets were very similar to those of the surrounding ground throughout the winter, although soil moisture was higher in the buckets than outside. This difference could at least in part be mitigated by drilling numerous additional holes in the bucket sides and bottom; we had a sufficient number of holes to provide basic drainage of the buckets, but having numerous additional small openings probably would result in soil conditions within the buckets being closer to those in the surrounding grassland or woodland. Very little is known about the overwintering ecology of American burying beetles, in part, because of the difficulty associated with studying them in their natural habitats. Simply having some basic information about factors affecting overwinter survival may be helpful in conservation efforts. Certainly, our study suggests that the species would have a higher probability of survival if carcasses are readily available as winter approaches. Acknowledgements We thank Sabrina M. Kirkpatrick, Elizabeth A. Phillips, and Daniel T. Farrer for assistance and oversight of the project, as well as for comments on the manuscript. Mary Clegert of URS Corporation provided funding coordination. The project was supported by the Military Department of Arkansas through URS Corporation. Appropriate permits were obtained from the U.S. Fish and Wildlife Service. We thank Michael Amaral and an anonymous reviewer for helpful suggestions concerning the manuscript.
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