Journal of Chemical Ecalogy, 1,1ol. 21, No. 9, 1995

RESPONSES OF BEAVER (Castor canadensis KUHL) TO PREDATOR CHEMICALS

A X E L E N G E L H A R T l and D. M ( 0 L L E R - S C H W A R Z E *

SUNY College of Environmental Science and Forestm, Syracuse, New York 13210

(Received January 6, 1995; accepted April 25, 1995)

Abstract--Free-ranging beaver (Castor canadensis) in two different beaver populations in New York State were exposed to predator chemicals to test feeding inhibition. Solvent extracts of feces were applied to stem sections of aspen, the preferred food tree of beavers, permitting smelling and tasting the samples. Predator odors were from wolf (Cants lupus), coyote (Cants latrons), dog (Canis familiaris), black bear (Ursus americanus), river otter (Lutra can- adensis), lynx (LytLr canadensis), and African lion (Panthera leo). The exper- iment was repealed. The predator odors reduced feeding compared to untreated or solvent-treated controls. One population consumed 17.0% of the samples with predator odor and 27.0% of the controls in summer, and 48.4% and 60.0%, respectively, in autumn. The other population accepted 3.15% of the predator odor samples and 11.05% of the controls in summer. Coyote, lynx, and fiver otter odors had the strongest effects. Diesel oil and bitter-tasting neem extract had weaker eflkcts. Predator odors are promising as feeding repellents lbr beaver.

Key Words--Adirondacks, Allegany State Park, allopatric, aspen, beaver, Castor canadensis~ feeding inhibition, Populus tremuhffdes, predator odor, repellent, sympatric.

INTRODUCTION

Popula t ions o f the Nor th A m e r i c a n b e a v e r (Cas tor canadens is Kuhl , 1820) are

current ly increas ing b e c a u s e low pelt p r ices d i s cou rage fur t rapping . T h e g r o w -

ing b e a v e r popu la t ions cause cons ide rab le wi ld l i fe d a m a g e by f lood ing roads ,

fores ts , and fields and by cu t t ing d o w n valuable t rees . This intensif ies the need

for ef fec t ive b e a v e r m a n a g e m e n t . A m o n g o t h e r m e a n s , e n v i r o n m e n t a l l y corn-

*To whom correspondence should be addressed. *Current address: Schulstr. 14, 71296 Heimsheim, Germany.

t 349

2751-3028/95/0900 1349507.50/0 ~ 1095 Plenum Publishing Corporation

1350 ENGELHART AND M OLLER-SCHWARZE

patible biological repellents are needed to keep beavers from sensitive areas or single trees. An obvious candidate for a natural repellent would be a potent predator odor (Mfiller-Schwarze, 1990).

Predator "s ign ," i.e., droppings, urine, scent marks, scrapes on the ground, scratches on objects, or rubbing sites, inform potential prey species about the presence, recent activity, and possibly diet of predators in an area. While avoid- ing predators, the prey species still has to operate in the same area. The use of predator odors as repellents is predicated on the assumptions that: (1) the prey species is merely alerted by the odor and avoids the particular spot or area in expectation of encountering a predator, and/or (2) the predator odor itself is aversive. In an application, the first case requires occasional reinforcement by an actual encounter with a predator. The second situation suggests a more lasting repellent effect, which also could be more general, across predator species. Sulfur-containing compounds, metabolites derived from protein, have been pos- tulated to be the aversive agent common to many predator odors (Mason, et al., 1994; Nolte et al., 1994). Trimethyl thiazoline from feces of red fox (Vulpes vulpes) is aversive to rats (Vernrt-Maury, 1992). Even plants rich in sulfur compounds, such as onion or leek, are avoided by herbivores such as black- tailed deer, Odocoileus hemionus columbianus, or goats (personal observations).

Previous predator odor studies on vertebrates have ranged from fish (Mathis and Smith, 1993) to mammalian herbivores such as black-tailed deer (M/.iller- Schwarze, 1972; Sullivan et al. , 1985b), white-tailed deer (Swihart et al. , 1991 ), red deer (Abbott et al . , 1990), and sheep (Amould, 1992, Amould and Signoret, 1993). Weldon (1990) has summarized the known responses of vertebrates to predator odors. Particularly relevant here are studies in lagomorphs (Sullivan and Crump, 1984; 1986; Sullivan et al . , 1985a; Boag and Mlotkiewicz, 1991, 1994), and rodents (B~iumler et al., 1990; Sullivan et al., 1988a,b, 1990a,b; Vemrt-Maury, 1992).

The primary mammalian predators of North American beavers are the wolf (Canis lupus) and coyote (C. latrans), particularly during spring and summer (Theberge et al. , 1978; Potvin et at. , 1988; Fuller, 1989) and when preferred prey such as white-tailed deer (Odocoileus viceinianus) are less abundant (Pim- lott et al., 1969).

It is thought that the decline of the beaver population on Isle Royale in Lake Superior around 1980 was caused by increased wolf predation (Shelton and Peterson, 1983). In northern Manitoba, wolves have been observed to stalk beaver (Nash, 1951 ). In several studies various amounts of beaver remains were found in wolf scats. On Isle Royale in Lake Superior, Mech (1966) reported that about 11% of wolf scats contained beaver hair. This compares with 7% in the Rocky Mountain national parks of Canada (Cowan, 1947) and 10.5% in Ontario (Peterson, 1955). In Algonquin Provincial Park, Ontario, up to 62.8% of wolf scats contained beaver hair in summer, but only 11.5% in winter (The-

BEAVER RESPONSES TO PREDATOR CHEMICALS | 35 |

berge et al., 1978). In Minnesota, however, 20--47% of wolf scats contained beaver remains in April and May, but only 2% in June and July (Fuller, 1989). In southern QuEbec, beaver constituted 29-44 % of biomass in the diet of wolves from May through November but only 1-3 % during the remainder of the year (Potvin et al., 1988). Indirect evidence for wolf predation on beaver comes from experimental wolf reduction in QuEbec, which resulted in an increase in beaver numbers and a decrease after the wolf population was allowed to grow again (Potvin et aL, 1992).

Coyotes have been observed to hunt and kill beaver in Rocky Mountain National Park, Colorado (Packard, 1940). In the Adirondacks, New York, coy- otes also prey on beaver (Brundage and Brocke, personal communication).

At Allegany State Park, New York, our group observed black bears (Ursus americanus) taking beaver out of live-traps on at least two occasions (Houlihan, unpublished; Schulte, 1993). Observations of black bears trying to dig into beaver colonies were "fairly common" in northern Saskatchewan (Gunson, 1970). Substantial predation by black bears has only been reported from an island in Lake Superior (Smith et al. , 1994). For grizzly bears (Ursus arctos) in Denali National Park, Alaska, Murie (198 t) had "'no observations suggesting bear predation on beavers." They may serve only as "occasional taste of carrion Ibr the bears ."

Fox (Vulpes vulpes), bobcat (Lyn_r rufus), and lynx (Lyn.r canadensis) prey little on beaver (Saunders, 1988). In a study in Maine, less than 5% of bobcat carcasses contained remains of beaver (Litvaitis et al., 1986). Despite claims in the past, the river otter (Lutra canadensis) is not a predator of beaver. Beaver are rare in the diet of otter. In a northeast Alberta area with high beaver and otter densities, Reid (1984) found only five otter scats among 1140 (0.4%) that contained beaver remains. Otter may have fed on beaver carcasses. No beaver remains were found in seven other studies of otter droppings, cited by Reid (1984).

The exclusively herbivorous beaver most prefers bark and leaves of aspen (Populus tremuloides and P. deltoides) among tree species. In our study areas they also feed on beech (Fagus grandifolia), speckled alder (AInus rugosa), red maple (Acer rubrum), yellow birch (Betula alleghaniensis), American hornbeam (Carpinus caroliniana), and other deciduous tree species. Conifers are rarely taken. Beaver also feed on grass, apples, ferns, and aquatic vegetation, depend- ing on the season.

Beavers are monogamous animals that live in families (for a review see Chapman and Fetdhamer, 1983). A typical family consists of an adult male and female and their offspring of the current and the past year. A family at a par- ticular site created by damming up a stream is termed a "'colony.'" For this study, a colony of beaver was the unit of experimental subjects.

In this study we seek answers to the following questions: Do predator odors

1352 ENGELHART AND M(JLLER-SCHWARZE

on or near food inhibit feeding by beaver? Are odors from certain predators more potent inhibitors than others? If so, are odors of predators sympatric with beaver more active than those from altopatric species?

METHODS AND MATERIALS

The study areas were Allegany State Park (ASP) in southwestern New York State and the Huntington Wildlife Forest (HWF) in the Adirondack Park in northern New York. The natural vegetation in both study areas is northeastern hardwood, with differences in the composition of the forest.

All odor samples except lion odor were prepared from excrement. The lion odor sample was prepared from a commercial lion urine extract (Imperial Chem- ical Industries PLC, Brachnell, England). All feces, except dog (a pet female black Labrador), were collected at the Burnet Park Zoo, Syracuse, For all sam- ples, 1 part feces (by weight) was suspended in 2 parts pure methanol for 2 hr and then filtered with a vacuum filter. The filtrate was used for the experiment, the solid phase discarded. The odor samples were stored in glass jars with alcohol-proof plastic lids in a refrigerator.

The aspen sticks used as carriers for the odors were cut from aspen saplings in the study area. Stems with a diameter of 1-2 cm and with as few lateral twigs as possible were selected. The sticks were cut fresh on the first day of each trial, pruned, and cut into sections 30 cm long. To facilitate uptake of the methanol solutions, the bark of all sticks, except the 'qntact" control, was perforated by rolling them on a nailboard. The sticks were dried at room tem- perature for 2 hr and then scented by dipping them to two thirds of their length into the extracts for 2 sec (except those left blank). In addition to intact and perforated blanks, some sticks were soaked in bitter-tasting extract of seeds (main component azadirachtin) of the neem tree, Azadirachta indica, which inhibits feeding by small rodents (B~iumler et al. , 1990). Some sticks were soaked in diesel oil, also a repellent for small rodents (B/iumler et al., 1990), and others were soaked in pure methanol as a solvent control. The sticks were dried for 2 hr before further handling.

For each trial we used 10 randomly chosen colonies. Twelve sticks, arranged in a row, were placed at the bank of each pond parallel to the water's edge near feeding places that were frequently visited by beavers. One stick each carried one of the seven predator odors, one neem extract, and diesel oil. The remaining three sticks served as controls: one was perforated and methanol-soaked, one perforated and untreated (blank), and one unperforated and untreated (intact). The distance between the sticks was 30 cm for the trials in June and July in ASP and in HWF. For the trials in October and November in ASP, the distance was increased to 1 m to determine whether distance affects the ability of the

BEAVER RESPONSES TO PREDATOR CHEMICALS 1353

beavers to distinguish the odors. The sticks were placed in a random order, determined by lot and the same pattern used for all 10 colonies. Each trial was five nights long, i.e., five beaver activity periods, without replacing any missing or altered sticks. This time period was long enough to assure the beaver had encountered the samples and short enough to minimize random influences such as heavy rains. First, a baseline trial with 12 intact, i.e., unperforated, untreated aspen sticks was run for three nights at 10 ASP colonies. At HWF, two such baseline trials were run (total number of sticks for baseline trials in both areas: 360). For treated samples, a total number of 2108 sticks were used. Their distribution over summer and fall, and ASP and HWF, the predator odors used, and the numbers of replications and colonies are listed in Table l.

The results of the nocturnal beaver activity were recorded each morning. Sticks were classified into completely peeled, partially peeled, left intact and moved, and left intact and in place. Missing sticks (swept away or sunken) were regarded as consumed by beaver (aspen wood does not float on water for a long time). Beaver sample sticks and often discard partially peeled sticks. Sticks that were peeled less than 80% were regarded as rejected, as were sticks that were not taken after five activity periods.

TABLE I . EXPERIMENTAL DESIGN: NUMBERS OF SAMPLES (NUMBERS OF TRIALS X

NUMBERS OF COLONIES) USED AT TWO BEAVER POPULATIONS AND

DURING DIFFERENT SEASONS

Population and Season

ASP summer H W F summer ASP fall Treatment [5 x 10) (5 x 10 + 1 × 4) (8 x 10) Total

River otter 54 80 Lynx 50 54 80 Coyote 50 54 80 Wolf 50 54 80 Dog 50 54 80 Black bear 50 54 80 Lion 50 54 80 Diesel oil 50 54 80 Neem 50 54 80 Methanol control 50 54 80 Intact 54 80 Blank 50 54 80

Number of treatments 10 12 12

Total number of sticks 500 648 960

134 184 184

184 184

184 184 184 184

184 134 184

2108

1354 ENGELHART A N D M U L L E R - S C H W A R Z E

As statistical tests of significance in the differences of numbers eaten vs. not eaten, we used the non-parametric Cochran and McNemar tests. They retain the pairwise comparison of simultaneous samples. X 2 tests were also used.

RESULTS

Allegany State Park (ASP). In a three-nights-long baseline test at the begin- ning of the trials, 74 of 120 (i.e., 12 sticks at each of 10 ponds) or 61.7% of intact aspen sticks were taken. For the trials run in June and July (sample size: 50 for each of 10 treatments) the percentages of experimental sticks accepted by the beaver after one to five activity periods are given in Figure 1. Acceptance ranged from 10.0% for coyote odor to 32.0% for the perforated aspen control (X 2 = 7.30: P < 0.01). (Intact, i.e., untreated, unperforated aspen logs, and

35

30

25

"~ 20 I -

E

10

/

1 2 3 4 5 Ac~vi~Periods

o

Wolf

Met;anol

Blan._k_ t

FIG. I. Responses by beaver {% samples taken) at Allegany State Park in June/July 1993.

BEAVER RESPONSES l ' O PREDAFOR CHEMICALS 1355

river otter odor had not been used at that t ime.) After coyote odor, the most active predator odors were lynx and black bear (16% of each accepted: X 2 =

0,236 vs. control: NS: black bear data not shown in Figure 1). Thus, coyote odor inhibited feeding signilicantly, compared with untreated controls.

In the October /November trials, significantly more sticks were consumed (Figure 2). This was a time of provisioning for the winter and reinforcing lodge

and dams. A total of 690 sticks were used, When only intact aspen sticks, 1 m apart, were offered, 48.7% were taken after three days. The most aw~ided odor was river otter (28% acceptance after three days: x 2 = 10.98; P < 0.001;

42.5% after five days), and the most frequently taken samples were the perfo- rated and methanol-treated aspen controls (63.7 % each: difference between otter and each control: X 2 = 7.26; P < 0.01). The wider spacing of 1 m between the sticks had no effect on the preference tier the controls. The ratio between the numbers of predator odor samples and controls that were consumed was

70

60

5O

1 -

40

~0

30

20

10

Coyote

Lynx

Lion

Wolf

Methanol

Blank

Otter

Intact

1 2 3 4 5 Activity Periods

FIG. 2. Responses by beaver at Allegany State Park in October/November 1993.

16

12

/

i - -

e,,

1356 ENGELHART AND Mt~ILLER-SCHWARZE

/

/

X ,̧̧ / / / / / : / / s

-/ > 4 - - :~: : ~/ . / /

/ /

Coyote

Lynx

Lion

Wolf !

Methanol

Blank

Otter

Intact

1 2 3 4 5 Activity Periods

FiG. 3. Responses by beaver at Huntington Wildlife Forest in August/September 1993.

0.81 in October/November. For an interstick distance of 30 cm, this relation was 0,49 for ASP in June/July and 0,30 for HWF in August/September (dif- ference not significant),

Huntington Wildlife Forest (HWF). At HWF (experiments during August/ September) the beaver consumed fewer sticks than at ASP. The acceptance rate ranged from 0 for river otter odor to 14.8% for the perforated aspen control (Figure 3; X ~- = 8.64; P < 0.025). This compares with 32.5% and 34.2% in two trials with only untreated perforated aspen sticks as baseline test (difference to otter: P < 0.001).

The ratio between the percentages of consumed predator-treated and control sticks at HWF was 0.30, Because the data were collected during the summer, the experiment was influenced by the fact that the beaver at HWF could choose from a great variety of available food, notably large beds of floating watershield (Brassenia sp.) leaves.

Both Study Areas. Figure 4 summarizes the responses in all trials in both areas. The average acceptance rate of five predator odors (those shown in the graphs) changed from 8.3% on the first day to 26.6% on the fifth, while the average for the three controls was 14.7% on day 1 and 38.5% on day 5. The average acceptance of five predator odors as percent of the average of the three

BEAVER RESPONSES TO PREDATOR CHEMICALS 1357

40

1 -

30

E

N 20

10

Y

2 3 4 5

Activity Periods

Coyot~

Lynx .=

Lion

Wolf

Methan,

Blank

Otter

Intact

FIG. 4. Summary of all responses in both study areas. (No data for river otter and intact controls for June/July).

controls increased slightly from 56.5% on day 1 to 68.1% on day 5. The most avoided predator odor (different odors in different blocks of trials) as percent of the average tbr the three controls increased gradually from 40.1% on the first day to 67.7% on the fifth. Table 1 summarizes the experimental design for all replicates in both areas, and Table 2 summarizes the results for all replicates in both areas.

The significance levels of the differences in the responses of the beavers to the different samples after five activity periods for all trials are shown in Table 3. The greatest statistical differences (P < 0.001) between predator odors and controls were as follows: all seven predator odors vs. perforated, untreated sticks; coyote, dog, otter, lynx, and lion vs. neem; black bear, coyote, dog, and otter vs. methyl alcohol; and coyote, otter, and lynx vs. diesel oil. Also significant (P < 0.01) were: wolf, lynx, otter, and lion vs. methyl alcohol: bear and wolf vs. neem; and lion vs. diesel oil. Among the controls, only blanks (unperforated, untreated) were taken significantly less often than untreated, but perforated sticks (P < 0.01).

Generally, there were no significant differences between different predator odors, The exception is the odor of otter, which was slightly, but consistently, more potent (P < 0.1) than all other predator odors except lynx. Although river

1358 ENGELHART AND MULLER-SCHWARZE

TABLE 2. SUMMARY OF A LL RESPONSES IN BOTH AREAS ( C u m u l a t i v e % E a t e n )

Night

Odors I 2 3 4 5

Lynx 9,7 10,8 14, I 20.1 23.9

Coyote 8,1 13.0 18.4 20, I 24.4

Lion 8, I 14.1 17.9 19.0 25,5

River otter 11. I 13.4 17, I 21.6 26. I

Black bear 10,3 14.6 18.4 23.3 26.6

Dog 7,6 12.5 16.8 23,6 27.7

Wol f 5,9 11.4 17.9 25,5 28.8

Diesel oil 14,4 20.6 26.0 28,8 33.6

Neem 1 1,4 18.4 25.5 29,3 35.3

Methanol control 16,8 26.0 30.9 3 I. 7 35.8

Intact 12,6 20.9 23.8 31,3 37,3

Blank 14.6 21.1 29.3 33.1 40,2

otter odor was the most avoided odor, there were treatments that were accepted less on average because river otter odor was not used for the June/July trials in ASP, when relatively few samples were taken. The only other slight differences among other predator odors occurred between coyote and lion odors (P < 0.1) and between lynx and lion odors (P < 0.1). The acceptance rates for neem and diesel oil were intermediate between predator odors and aspen controls (Table 2).

TABLE 3. SIGNIFICANCE LEVELS OF DIFFERENCES IN RESPONSES TO SAMPLES AFTER

FIVE ACTIVITY PERIODS FOR ALL TRIALS a

W o l f Coyote Dog Otter Lynx Lion D N I M B

Bear . . . . * - - * * * - *** ***

Wol f - * - - * ** - ** ***

Coyote - * - * *** *** - *** ***

Dog * - - * *** - *** ***

Otter - * *** *** * *** ***

Lynx * *** *** - ** ***

Lion ** *** - ** ***

Diesel oil . . . . *

Neem - *

Intact * **

Methanol

"Abbrevia t ions for odors: D: Diesel oi l : N: neem: I: intact: M: methanol , B: blank (perforated). ***P < 0+001; **P < 0 .01: *P < 0.1; - : P > 0.1

BEAVER RESPONSES TO PREDATOR CHEMICALS 1359

DISCUSSION

The responses toward the samples show that free-ranging beaver are able to distinguish between different odor treatments of food, which in this experi- ment included the opportunity to taste the samples. They did so in the presence of abundant alternate food. This type of field experiment contrasts with captivity or laboratory studies in which the experimenter provides the only food available and manipulates its amount. Examples are experiments with cattle (Pfister et al., 1990), sheep (Arnould and Signoret, 1993; Pfister et al., 1990), goats (Weldon et al. , t993), or mountain beaver (Epple et al. , 1993). The three questions posed at the outset can be answered as follows. At least some predator fecal extracts inhibit feeding (the actual concentrations of active compounds are unknown at this point). The effects of different extracts did not differ signifi- cantly from one another. From this it follows that there was no significant difference between chemicals of predators that are sym- or allopatric with beaver.

The different responses to the samples by the beavers in the two regions may result from genetic differences between the two populations or environ- mental factors such as experience with predators or the composition of the food supply. Originally there were two different subspecies in the two respective study areas (Hall, 1981). The original subspecies in the Adirondacks was Castor canadensis acadicus Bailey and Doutt (Hall, 1981). The subspecies for western New York State, including ASP, is the nominate race. The beaver had been almost extirpated in the entire State of New York in the 19th century. The Adirondack population was restocked in 1905 with seven beaver from Canada (nominate race), and again in 1907, when 14 specimens from Yellowstone National Park (subspecies C. c. missouriensis Bailey) were released at Old Forge. After their extirpation, the first beavers at ASP were recorded in 1937 (Shadle and Austin, 1939). These beaver had come north from Pennsylvania where animals from Wisconsin had been introduced in 1917 and subsequent years (Hilfiker, 1991). Still, the genetic distance between the two current study populations is not known.

Since the two study areas also differ in the presence of potential predators, the effect of learning could be important. In general, ASP has fewer different predators. Fetidae are totally missing (personal communication with local wild- life managers) and so are wolves. Black bear, coyote, and river otter occur in the park (personal observation of animals and tracks by both authors). By con- trast, all North American predators whose odo~ were used, except wolf, occur in HWF. The lynx was extirpated in the Adirondacks in the late 19th century and recently reintroduced (Brocke et at., 1991), but is still very rare. The closely related bobcat (Lyn_r rufus) also occurs in the Adirondacks (Saunders, 1988). Black bear tracks and droppings around beaver ponds have been seen in HWF by the author, as have three specimens of river otter and several coyotes. The

1360 ENGELHART AND MOLLER-SCHWARZE

barking and howling of coyote packs was often heard. The abundance of pred- ators in HWF could explain why the predator odors were avoided so strongly, as were the nearby control samples. Nevertheless, beavers did not avoid the odors of sympatric species significantly more than the odor of the allopatric lion. However, the slightly more avoided odors were those of species that are sym- patric with each particular beaver population used in this study, such as river otter and lynx in HWF.

Other studies of predator odor effects on feeding by herbivores show con- sistent effects (e.g., Mfiller-Schwarze, 1972; Sullivan and Cramp, 1984). Dog odor has no significant effect on the feeding behavior of snowshoe hare (Sullivan et al. , 1985a), but coyote odor decreases browsing by black-tailed deer signif- icantly (Sullivan et al., 1985b). Black-tailed deer avoid the odors of sympatric predator species more than those of allopatric species. This behavior may have a genetic basis but might be refined by learning (Miiller-Schwarze, 1972). In this study beavers avoided the odors of sympatric predators such as river otter and coyote that actually occur within the range of the tested beaver slightly more than those of originally sympatric, but now absent, species such as the wolf. Lynx are in the same category as wolf (except for recent local reintroductions) (Brocke et al. , 1991), but their odor was still avoided. Furthermore, beaver do not discriminate between the odors of the allopatric lion and the sympatric wolf, nor did they distinguish between wolf and dog odor. Similarly, Mason et al. (1994) found that urine odors from dog, mink, bobcat, and coyote inhibited feeding by mountain beaver, Aplodontia rufa, equally well. These authors pos- tulate that to herbivores, sulfur compounds constitute a general predator cue across carnivore species.

We have evidence that beavers actually encounter predators in our study areas. The authors observed river otters in beaver ponds in both regions. Black bear footprints and droppings close to beaver ponds were found in ASP and HWF. In our team's studies, a black bear took a beaver out of a Hancock live- trap in ASP on two occasions (Houlihan, unpublished; Schutte, 1993). Beavers might learn to avoid predator odors through direct encounters or witnessing attacks on other beaver. A beaver might also be conditioned by warning signals from conspecifics, even though the signal is associated only with a predator odor, not an encounter itself.

The seasonal differences in sample acceptance are most likely correlated with the changing abundance of palatable food. In summer beavers feed very little on tree bark. Beavers prefer to eat leaves and chew the bark of a twig only after all leaves are consumed. They also eat grass and forbs. This might explain the low interest in the aspen sticks in general at both ASP and HWF in summer. In September the situation changes dramatically. The beavers cut many trees to build food caches for the winter. Furthermore, beavers working on bulky food items such as branches might entirely ignore the relatively small aspen samples.

BEAVER RESPONSES TO PREDA-FOR CHEMICALS | 361

During this period they spend more time than usual on the shore and are more exposed to predators. They might be more alert and are consequently avoiding the predator odor more for both of these reasons. The responses at HWF dropped towards zero acceptance from the middle of September onwards. In late autumn the growing season is over, and beavers depend almost exclusively on bark in their diet. The aspen samples might then become more attractive again and the beaver less selective.

When the distance between the sticks was increased from 30 cm to t m, the beaver did not discriminate controls more from predator odors. Thus "olfac- tory overshadowing" may not have been important with our arrangement of the samples.

During some days in late October the ponds were frozen, and the beaver tended to either ignore or accept all samples. The ice cover affected the beavers' activities, and the low temperature of air and sticks could have impaired their ability to distinguish between different odors. The different amounts of rainfall in the course of the year could also play an important role. Since the predator odors were applied as alcoholic solutions, they are easily washed away by rain. Sticks with predator odor that had lain in the water for some time were eventually chewed. The same was true for initially rejected sticks with diesel oil. In other studies, such as that of black-tailed deer (Sullivan et al., 1985b), predator odors also became less effective after heavy rains. The strong feeding responses after rainfall indicate that the odor was washed away. This might be different for each odor, depending on original odor strength and other compounds present. For instance, wolf odor was more avoided than any other odor on the first day (Figure 1) but had no strong repellent effect later on. The reverse was true for river otter odor. That taste, in addition to olfaction, may be involved is shown by the fact that beaver often consumed more than half of the bark on a stick and then abandoned the rest.

Any application of repellents has to take into account which predator spe- cies are present in the area. Beaver exposed to a more diverse predator guild may avoid more strongly repellents based on predator odors. For lasting effects, the learning ability of beaver requires that other stimuli be used to reinforce the avoidance of predator odors. Furthermore, odors applied directly to food may trigger responses different from odors placed in the vicinity of food, and the senses involved determine the stimuli used. For an effective beaver repellent to last in the elements, a formulation with a hydrophobic carrier will be necessary. The next step is the chemical isolation and identification of the active com- pounds.

Acknowledgments--We thank Drs. Rainer Brocke and William Porter of the Adirondack Wild- life Program for partially funding this research: Mr. Richard Sage, Assistant Director of the Adi+ rondack Ecological Center, and Mr. James Rich, Regional Director of ASP, [br administrative support; Ms+ Kathryn Burlington for arranging the loan of night vision goggles; Capt. Paul Cloutier

1362 ENGELHARF AND MOLLER-SCHWARZF.

of the Division of Military and Naval All;airs in Latham for loaning night vision goggles; and Stall" Sgt. Norman Pmvoncha of the Ticonderoga Armory Ii~r providing the goggles and instruction Ior their use. Messrs. Michael Rehberg and Lixing Sun helped with the lieltl work and gave nluch useful advice. Mr. Allen Baker from Burner Park Zoo provided predator samples, and Mr. Chris- topher Sack helped in the laboratory, Prof. Dr, R, Apfelbach, University of Ttibingen, Germany, referred A.E. to ESF. We thank Drs. Roberl M, Silverstein and Stephen Teale liar critical reading of the manuscript.

REFERENCES

ABBOTT, D.H., BAINES, D.A., FA~t_KJ~S. C.G., JENKINS, D.C.. NING, P .C .YK. . and T()MLINSON, A.I. 1990. A natumI deer repellent: chemistry and behaviour, pp, 599-609, in D. Macdonald, S. Natynczuk. and D. M{iller-Schwarze. (eds.), Chemical Signals in Verlebmtes Vol. 5, Oxli~rd University Press, New York,

AnNOtU_D. C. 1992. Repulsion alimentaire chcz les ongules. Thesis. Universitd de Paris VItl, Biologie des organismes, Paris, November 1992.

ARN~tII_I). C,, and SIGN~RI~t. J.-P. 1993. Sheep fi:~od repellents: ellicacy of various products, habituation, and social facilitation. J. Chem. Ecol. 19:225-236.

B.at:M~.F.R, W.. MIE~.K~. H.. and ZAHY1-:R, V, 1990, Behandlung yon Eicheln rail Repellentien gegen Nagetierschiiden. Ariz. Schaedlineskde. Pflanz. Umn'ehschutz 63:15 19.

BOAG, B., and MLOT~m~WlCZ. J.A. 1991. Evaluation of an odour derived from lion faeces on the behaviour of wild rabbits. Ann Appl, Biol. I 18{Suppl, t: 18-19,

BOAG, B., and Mt_trrKlkWlCZ, J,A. 1994. Effect of odor derived from lion lieces on behavior of wild rabbits. J. Chem. Ecol. 20:631-637.

BROCKF, R., GUSTAVSON, K,A., and FOX, LB . 1991. Restoration of large predators: Potential and problems, pp. 303-315. in D.J, Decker, M,E, Krasny, G,R, Goff, C.R. Smith, and D.W. Gross (ed.). Challenges in the Conservation of Biological Resources: A Practitioner's Guide. Westview Press, Boulder, Cnlorado.

CHAPMAN, J.A., and FFI.DHAMER, G,A. (eds,), 1983, Wild Mammals of North America. The Johns Hopkins University Press, Baltimore, pp. 256-281,

CowaN, I.M. 1947. The timber wolf in the Rocky Mountain national parks of Canada. Can. J. Res. 25: 139-174.

EPPLE, G., MASON, R.J., NOLTE, D,L.. and CAMPBt~LL, D,L. 1993. EITectss of predalor odors on lieeding in the mountain beaver (Aplodoulia rufil), ,1, Mammal, 74:715-722.

FULLISR, T,K. 1989. Population dynamics of wolves in norlh-central Minnesota. Wihll. Mono,~r. 105:1 41.

GUNSON. J.R. 197(I. Dynamics of the beaver of Saskatchewan's northern forest. MS thesis. Uni- versity of Alberta, Edmonton, Alberta, Canada, 122 pp.

HALL, E.R. 1981. The Mammals of North America, 2nd ed. Wiley, New York. HILFLKI~R, E.L. 1991. Beavers: Water, Wildlife and History. Windswept Press, Interlaken, New

York. 198 pp. L~TVAmS, J.A., CLARK, A.G.. and HIFN'r. J.J. 1986. Prey selection and fat deposits of bobcats

{Fetis rufus) during autumn and winter in Maine. J. Mammal. 67(2}:389-392. M/~SON, J.R., EI'I,Lk, G., and Nog'rtl, D.L. 1994. Semiochemicals and improvements in rodent

control, pp. 327-345, in B.E. Galef, P. Valsecchi, and M. Mainardi Ieds.). Behavioral Aspects of Feeding: Basic and Applied Research in Mammals. Harwood Academic Press. London.

MATU~S, A. and SMITH, J.F, 1993. Fathead minnows, Pimephales promelas, learn to recognize northern pike, Esox lucius, as predators on the basis of chemical stimuli from minnows in the pike's diet. Anita. Behav. 46:645-656.

BEAVER RESPONSES TO PREDATOR CHEMICALS 1363

MECH, L.D. 1966. The wolves of Isle Royale. Fauna Natl. Parks U.S. Ser. 7:210 pp. MOI.LEr-ScHwAI~ZE. D. 1972. Responses of young black-tailed deer (Odocoileus hernionus col-

umbianusl to predator odors. J. Mammal. 53:393 598. MOLLER-SCHWARZE, D. 1990. Leading them by their noses: animal and plant odors for managing

vertebrates, pp. 585-598, in D.W. Macdonald, D. M/Jller-Schwarze, and S.E. Natynczuk (eds.). Chemical Signals in Vertebrates Vol. 5. Oxford Univ. Press, Oxford.

Murm. A. 198t. The Grizzlies of Mount McKinley. U.S. Department of the Interior, National Park Service, Washington, D.C. 251 pp.

NASH, JB. 1951. An investigation of some problems of ecok,gy of the beaver Castor eanadensis Kubl in northern Manitoba. MS thesis. University of Manitoba. 64 pp.

NoL'r~, D.I., MASON, J.R., EPPLE, G., ARONOV, E., and CAMPBI-',LL, D.L, 1994. Why are predator urines aversive to prey? J. Chem. Ecol. 20:1505-1516.

PACKARD, F.M. 1940. Beaver killed by coyotes. J. Mammal. 21:359-360. PETERSON, R.L. 1955. North American Moose. University of Toronto Press, Toronto. 280 pp. PFISTER, J.A., Mt~I.t_ER-SCHWARZF., D., and BAkPf-t, D.F. t990. Effects of predator fecal odors ,m

feed selection by sheep and cattle. J. Chem, Eeof 16(2):573-583. PIMLO'I-r, D.H., SHANNON, J.A., and KII.ENOSKY, G.M. 1969. The ecology of the timber wolf in

Algonquin Provincial Park. Ontario Department of Lands and Forests Research Report (Wild- life) No. 87, 92 pp.

POTVIN, F., JOI.ICOEUR, H., and HtI~T, 1. t988. Wolf diet and prey selectivity during two periods lot deer in Qu6bec: Decline versus expansion. Can. J. ZooL 66: 1274-1279.

Po'rvln, F., BRETON, L., Pn.on, C., and M~,o)t aRr, M. 1992. Impact of an experinaental wolf redaction on beaver in Papineau-Labelte Reserve, Qudbec. Can. J. Z~of 70:180-183.

REID, D.G. 1984. Ecological interactions of river otter and beavers in a boreal ecosystem. MS thesis. University of Calgary, Calgary, Alberta, Canada. t99 pp.

SAUNOI-:I~S, D.A. 1988. Adirondack mammals: State University of New York, College of Environ-

mental Science and Forestry, Syracuse. N.Y., 216 pp. SCHUI.TI~, B.A. 1993. Chemical communication and ecology of the North American beaver (Castor

canadensisL PhD dissertation. State University of New York, College of Environmental Sci-

ence and Forestry, Syracuse, New York. 194 pp. SHADI.~, A.R., and AUSTIN, T.S. 1939. Fifteen months of beaver work at Allegany State Park,

N.Y.J. Mammal. 20:299-303. SttELT()N, P.C., and PETERSON, R.O. 1983. Beaver, wolf and moose interactions in Isle Royale

National Park, USA. Acta Zool. Fen,. 174:265-266, SMrrH, D.W., TRAtlBA. D.R., ANDt~rSON, R.K., and Pr!T~!RSON, R.O. 1994. Black bear predation

on beavers on an island in Lake Superior. Am. MidI. Nat. 132:248-255. SUt.LIVAN, T.P., and CRt~MT', D.R. 1984, Influences of mustelid scent gland compounds on sup-

pressing of feeding by snowshoe hares (Lepus ametqcanus). J. Chem. Ecol. 10:1809-1821. SULLIVAN, T.P., and CRUMP, D.R. 1986. Feeding responses of snowshoe hares (Leptts ameFicamts)

to w~latile constituents of red lox (Vulpes wdpes) urine. J. Chenl. Ecol. 12:729-739. St~LLIVAN, T.P., NOrDSTROm, L.O., and SULLIVAN, D.S. 1985a. Use of predator odors as repellents

to reduce feeding damage by herbiw~res. 1. Snowshoe hares (Lwus americanus). J. Chem,

Ecol. 11:903-919. SULLiVAn, T.P., NORDS'rro~,~. L.O., and SULL~V,*,N, D.S. 1985b. Use of predator odors as repellents

to reduce feeding damage by herbivores. 11. Black-tailed deer (Odoeoileus hemionus cohlm-

hiamts). J. Chem. Ecol. t1:921 935. SULLiVaN, T.P., fRUMP, D.S., and SUkLIVAN, D.S. 1988a. Use of predator odors as repellents to

reduce I~.eding damage by herbivores. 111. Montane and meadow voles (Mierotus numtanus and Mierotus pem*syh'anicus). J. Chem. Ecol. 14:363-377.

SULliVAN, T.P., CRUMP, DR., and SULLIVAN, D.S. 1988b. Use of predator odors as repellents to reduce feeding damage by herbivores. IV. Northern pocket gophers {77umumO's talpoides). J. Chem. Ecol. 14:379-389.

1364 ENGELHART AND MOLLER-SCHWARZE

SULLIVAN, T.P., fRUMP, D.R., WIESER, H., and DIXON, E.A. 1990a. Responses of pocket gophers ~Thomomys talpoides) to an operational application of synthetic semiochemicals of stoat (Mus- tela erminea). J. Chem. Ecol. 16:941-949.

SULLIVAN, T.P., CRUMP, D.R., WlESF.ZR, H., and DIXON, E.A. 1990b, Comparison of release devices for stoat ~Mustela erminea~ semiochemicals used as montane vole repellents. J. Chem. Ecol. 16:951-957.

SWIHART, R.K., PIGNATEI.LO, J.J., and MAqqqNA, M.I, 1991. Aversive responses of whitc-tailed deer, Odocoileus virginianus, to predator urines. J. Chem, Ecol. I7:767-777.

THEnERGI:. J.B., OOSENBRUG, S.M., and PIMI_OTT, D.H, 1978. Site and seasonal variations in food of wolves, Algonquin Park, Ontario. Can. Field Nat. 92:91-94.

VERNFT-MAURY. E. 1992. Un d6clencheur kairomonal de I'alarme et de 1"6vitement, le trimflhyl- thiazoline, analyse chimio- et neuro6thologique. Thesis. Universit,5 Claude Bernard, Lyon 1, Lyon. September 1992.

WEt_DON, P.J. 1990. Responses by vertebrates to chemicals from predators, pp. 500-521, in D.W. Macdonald, D. M~iller-Schwarze, and S.E, Na~ynczuk (eds.). Chemical Signals in Vertebrates 5. Oxford University Press. Oxfi~rd.

WELl)ON, P.J., GRAHAM, D.P., and MEARS, L.P. 1993. Carnivore fecal chemicals suppress feeding by Alpine goats (Capra hircus). J. Chem. Ecol. 19:2947-2952.