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Surplus-killing by endangered San Joaquin kit foxes (Vulpes macrotis mutica) is linked to a local population decline of endangered giant kangaroo rats (Dipodomys ingens).

Surplus-killing occurs when a predator kills more prey than it can eat, leaving carcasses unconsumed (Kruuk, 1972; Meuller and Hastings, 1977). Although surplus-killing has been documented in predators ranging from canids to birds of prey (Nunn et al., 1976), the frequency and extent of this behavior among individual predators is unknown. Additionally, the effects of surplus-killing on the population dynamics of prey are poorly studied. We report surplus-killing of giant kangaroo rats (Dipodomys ingens) by a family of San Joaquin kit foxes (Vulpes macrotis mutica) in the Carrizo Plain National Monument, california, and explore the ecological causes and consequences of this event.

On 25 May 2011, 91 carcasses of the giant kangaroo rat were found at two dens, located ca. 30 m apart, of the San Joaquin kit fox. The carcasses appeared to have been ejected from the dens, with 61 carcasses found near a den on one of our study plots and 30 carcasses counted at the second den (Fig. 1). A family of San Joaquin kit foxes with at least three juveniles and two adults was seen near these dens during spotlighting-surveys conducted on 16, 17, and 19 May 2011. Kit foxes maintain multiple active dens, with an average home range in the Carrizo Plain of 11.9 [km.sup.2] (White and Ralls, 1993). Thus, both dens were likely used by a single family of San Joaquin kit foxes. The majority of carcasses of the giant kangaroo rat were intact with no signs of consumption, and they ranged in condition from freshly killed to mummified. It is unknown how long the bodies had been stored underground. Observers noted that carcasses were still at the entrances of dens in August, and they emitted a strong rotting odor.

We documented these surplus-killings as part of a long-term study in the Carrizo Plain to understand relationships among giant kangaroo rats, cattle grazing, and other species in a grassland community. The surplus-kills were found on and immediately adjacent to one of our 30 study plots where a variety of surveys are conducted each year, including biannual mark-recapture surveys of giant kangaroo rats. Each study plot is 140-x-140 m in size (1.96 ha). Trapping occurs in April and August for three consecutive nights on each plot (see Prugh and Brashares, 2010, for details of the trapping protocol). Our study was approved by the University of California Animal Care and Use Committee (R304) at the University of California, Berkeley, and followed guidelines of the American Society of Mammalogists (Sikes et al., 2011).

Giant kangaroo rats are a primary food for San Joaquin kit foxes in the Carrizo Plain, where they are the most common nocturnal rodent (Grinnell et al., 1937; McGrew, 1979; Prugh and Brashares, 2012). Giant kangaroo rats completely dominate the community of nocturnal rodents in our study area; only 29 of 24,895 captures from 2007-2012 were of species other than D. ingens. Although locally abundant, the giant kangaroo rat and San Joaquin kit fox are federally endangered due to extensive loss of habitat (United States Fish and Wildlife Service, in litt.). Thus, insight into the predator-prey dynamics between these species may aid the development of plans for their recovery.

San Joaquin kit foxes have been studied extensively in the Carrizo Plain and surrounding areas (e.g., White and Ralls, 1993; White et al., 1996; White and Garrott, 1997, 1999; Cypher et al., 2000). In the mid-1990s, during a year of unusually high density of kangaroo rats, observers found carcasses of kangaroo rats ejected from several natal dens in the nearby Elk Hills (B. Cypher, pers. comm.). However, no more than a dozen carcasses were found at any given den, and the heads of the carcasses had been consumed. Our observation of 91 ejected carcasses from two nearby dens is, therefore, an unusually large surplus-killing event for this species. In addition, this is the first case of surplus-killing we have discovered in 5 years of intensive fieldwork. Thus, surplus-killing does not appear to be a widespread behavior among San Joaquin kit foxes.

If carcasses are not ejected from dens, then surplus-killing may remain undetected. However, we suspect foxes would eject carcasses in most cases due to the stench and parasitic outbreak that would result from dozens of rotting carcasses. Additionally, the entrances of dens remain littered with bones of giant kangaroo rats 2 years after the event, indicating that these events should be detectible for a long period of time. While canids often cache prey for later use by themselves or their pups (Samelius and Alisauskas, 2000), these caches were not utilized in the case we report.

Three factors have been proposed as triggers of surplus-killing events: severe weather; poor condition of prey; super-abundant prey. Surplus-killing is often linked to environmental conditions, such as deep snows or heavy storms (Patterson, 1994). These conditions can impede the ability of prey to escape and hide from predators. Additionally, extreme weather or chronic shortage of food can drive prey to engage in behavior that exposes them to a high risk of predation (Delgiudice, 1998). However, these factors are not always associated with surplus-kills. For example, Miller et al. (1985) found in their observation of surplus-killing by wolves (Canis lupus) that depredated calves of caribou (Rangifer tarandus) were in good physical condition. In addition, when prey are unusually abundant, their increased presence may trigger predation past the point of satiation (Miller et al., 1985). Kruuk (1972:12) argues that "satiation in carnivores does not inhibit further catching and killing, but it probably does inhibit searching and hunting. Thus carnivores are able to procure an 'easy prey' but normally satiation limits numbers killed."

Of the three potential triggers, super-abundant density of giant kangaroo rats is the most likely cause of the incident of surplus-killing we report. Density of the giant kangaroo rat was estimated in trapping sessions during April and August each year using the robust design with heterogeneity estimator in program RMark (J. Laake and E. Rexstad, http://www.phidot.org/software/mark/ docs/book). The density of giant kangaroo rats on the plot where the surplus-killings occurred (plot C5) increased by 34% between August 2010 and April 2011. The dynamics of the giant kangaroo rat on plot C5 reflected a general trend across all 30 sites; the average density of giant kangaroo rats increased by 35% during this time period (from 38 giant kangaroo rats/ha to 52/ ha; R. L. Endicott and L. R. Prugh, in litt.). Densities in April 2011 were significantly higher than in any previous year of the study (Fig. 2), and survival over winter was highest between August 2010 and April 2011. Giant kangaroo rats were, therefore, unusually abundant in April 2011.

There were no apparent plot-specific environmental conditions or events of extreme weather that would have rendered giant kangaroo rats on plot C5 especially vulnerable to predation. Additionally, giant kangaroo rats captured on plot C5 during our live-trapping sessions had similar body condition (as measured by the ratio of the body weight to the skull length) as giant kangaroo rats captured on our other plots. The average body-condition index of adults on C5 in April 2011 was 2.84 (n = 52; 95% confidence interval, CI, = 2.79-2.89), and the average condition of adults on all 30 plots combined also was 2.84 (n = 1,380; 95% CI = 2.83-2.85). It is possible that a research-effect may have increased activity of foxes on our plots, because San Joaquin kit foxes are drawn to novel items such as Sherman traps and plot stakes (B. Cypher, pers. comm.). However, this issue should have affected all our plots equally.

The consequences of surplus-killing for populations of prey have not been previously reported. We used our mark-recapture dataset to examine the change in density of the giant kangaroo rat following the surplus-kills. Of our 30 plots, the plot where surplus-killing was observed (C5) had the largest decline in density between the April and August 2011 trapping sessions, from 56 individuals/ ha in April (95% CI = 56-58) to 31/ha in August (95% CI = 29-34; Table 1). Densities on a paired plot (E5) located 60 m away, in contrast, were 52 in April (95% CI = 52-54) and 42 in August (95% CI = 41-45). Densities of the giant kangaroo rat also sharply declined on plot E1 (Table 1), which was located several kilometers from plot C5, and on which no surplus-kill was detected. However, a family of San Joaquin kit foxes had active dens on plot E1, so heavy predation also may have been involved in that decline.

The fact that populations of giant kangaroo rats declined on plots such as E1, where no surplus-kill was found, raises the possibility that heavy predation rather than surplus-killing caused the steep decline observed on plot C5. Indeed, populations on plots often declined between April and August across all 5 years of our study (2008-2012), though the average decline was minimal (Table 1). The population of giant kangaroo rats on plot C5 was unusual in that it declined from April-August during each of the 5 years and had the steepest average decline among the 30 plots (Table 1). Thus, dynamics on this plot appear to differ from those on other plots.

To further examine the possibility that the steep declines on plot C5 could have been caused by heavy predation rather than surplus-killing, we evaluated the dynamics of giant kangaroo rats on each plot in relation to the distance to the nearest known natal den or family group of San Joaquin kit foxes from 2008-2012. If populations of giant kangaroo rats tend to steeply decline on all plots close to natal dens of San Joaquin kit foxes, this would indicate that heavy predation rather than surplus-killing may have caused the local decline observed on plot C5. Active dens were recorded opportunistically by project-staff each year. Additionally, locations of family groups were recorded during spotlighting surveys conducted during four consecutive nights in May and July each year. We used a hierarchical linear model to examine the effect of distance to nearest den or sighting on the change in density of the giant kangaroo rat from April-August on each plot each year. Distances were log-transformed prior to analysis. Year was entered as a random effect, plot was entered as a nested (within year) random effect (Pinheiro and Bates, 2000), and analyses were conducted using the lme function in program R.

We found no relationship between distance to the nearest den or sighting of the San Joaquin kit fox and change in density of the giant kangaroo rat (Fig. 3; [F.sub.1,134] = 0.70, P = 0.40). Thus, local declines in populations of the giant kangaroo rat do not appear to be caused by proximity to natal dens of San Joaquin kit foxes.

While other factors may have been involved in the steep decline in the density of giant kangaroo rats on plot C5, it is likely that surplus-killing by one family of San Joaquin kit foxes played a major role. Our finding supports previous studies documenting strong impacts of individuals or small groups of predators (Linnell et al., 1999). For example, a single cougar (Puma concolor) killed 9% of the adults and 26% of the lambs in a population of bighorn sheep (Ovis canadensis) in Alberta during a single winter (Ross et al., 1997). Our observation indicates that surplus-killing by a small group of predators can similarly have a marked impact on the dynamics of populations of targeted prey. Because cases of surplus-killing may occur sporadically and are difficult to document, it is unknown how widespread this behavior may be among individual predators and how often such incidents occur. Our findings highlight the importance of long-term and large-scale studies in the field for documenting events such as surplus-killing because these rare events may have stronger ecological impacts than previously thought.

Funding and logistical support was provided by the Bureau of Land Management and the United States Department of Agriculture. We thank assistants in the field who collected data for this study (S. Kong, A. Ross, G. Taylor, R. Lyon, and A. Matea). B. Cypher and an anonymous reviewer provided helpful comments on an earlier version of this manuscript. L. Withey translated the abstract into Spanish.

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Submitted 28 November 2012. Acceptance recommended by Associate

Editor Jennifer K Frey 20 May 2013.

RACHEL L. ENDICOTT, LAURA R. PRUGH, * AND JUSTIN S. BRASHARES

Department of Environmental Science, Policy, and Management, 137 Mulford Hall, University of California, Berkeley, CA 94720 (RLE, JSB)

University of Alaska Fairbanks, Institute of Arctic Biology, Fairbanks, AK 99775 (LRP)

* Correspondent: lprugh@alaska.edu

TABLE 1--Density (number per hectare) of giant kangaroo rats
(Dipodomys ingens) on 30 study plots in the Carrizo Plain National
Monument, California, during 2011, and average change in density from
April-August during 5 years (2008-2012). The first 20 plots were part
of a study of grazing by cattle, and an additional 10 plots were
located in an ungrazed pasture. Mark-recapture estimates, with 95%
confidence intervals (CI) in parentheses, are given as well as the
change in density over time.

Plot        Plot      Density estimate (95% CI)
          treatment

                      April 2011   August 2011

C1        Grazed      54 (52-59)   57 (54-64)
E1        Ungrazed    41 (40-45)   20 (18-24)
C2        Grazed      54 (53-58)   69 (68-73)
E2        Ungrazed    55 (53-61)   52 (50-59)
C3        Grazed      54 (53-58)   61 (59-66)
E3        Ungrazed    54 (53-57)   48 (46-52)
C4        Grazed      40 (39-42)   63 (61-66)
E4        Ungrazed    46 (45-49)   60 (58-64)
C5        Grazed      56 (56-58)   31 (29-34)
E5        Ungrazed    52 (52-54)   42 (41-45)
C6        Grazed      40 (39-43)   32 (31-36)
E6        Ungrazed    50 (49-52)   35 (34-39)
C7        Grazed      47 (46-51)   55 (53-61)
E7        Ungrazed    52 (50-58)   55 (52-62)
C8        Grazed      52 (51-55)   68 (66-72)
E8        Ungrazed    58 (57-61)   64 (62-69)
C9        Grazed      48 (47-50)   62 (60-66)
E9        Ungrazed    44 (44-46)   43 (42-46)
C10       Grazed      73 (71-76)   73 (70-78)
E10       Ungrazed    63 (62-66)   72 (69-76)
S1        Ungrazed    57 (56-59)   71 (70-75)
S2        Ungrazed    73 (73-75)   51 (49-54)
S3        Ungrazed    56 (55-59)   60 (58-64)
S4        Ungrazed    56 (55-58)   54 (53-58)
S5        Ungrazed    51 (50-53)   35 (34-39)
S6        Ungrazed    50 (49-53)   38 (37-41)
S7        Ungrazed    58 (57-64)   58 (57-64)
S8        Ungrazed    31 (31-33)   24 (23-26)
S9        Ungrazed    35 (35-37)   33 (32-35)
S10       Ungrazed    52 (51-54)   43 (42-46)
Average               52 (49-55)   51 (46-56)

Plot      Change in      Mean
           density      change
           in 2011    in density
                      2008-2012

C1             3          5.0
E1           -22         -3.8
C2            15         -8.8
E2            -3         -5.0
C3             7          1.4
E3            -6         -4.4
C4            23         -3.0
E4            14         -9.4
C5           -26        -18.2
E5           -10        -12.4
C6            -8        -12.0
E6           -15        -14.0
C7             8         -6.8
E7             3         -3.6
C8            16         -2.6
E8             6          2.2
C9            14          5.8
E9            -1          0.6
C10            0          2.0
E10            9          5.6
S1            14         -0.6
S2           -23         -5.8
S3             4         -7.2
S4            -1         -5.4
S5           -15         -6.6
S6           -12         -2.0
S7             0          5.0
S8            -8          5.6
S9            -3          5.2
S10           -9         -0.8
Average       -1         -3.0
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Title Annotation:NOTES
Author:Endicott, Rachel L.; Prugh, Laura R.; Brashares, Justin S.
Publication:Southwestern Naturalist
Article Type:Essay
Geographic Code:1USA
Date:Mar 1, 2014
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