Behavioral Ecology Vol. 13 No. 3: 381-385
© 2002 International Society for Behavioral Ecology
Use of California bay foliage by wood rats for possible fumigation of nest-borne ectoparasites
a Department of Biology, Vassar College, Poughkeepsie, NY 12604, USA b Department of Anatomy, Physiology and Cell Biology, School of Veterinary Medicine, University of California, Davis, CA 95616, USA
Address correspondence to R.B. Hemmes. E-mail: hemmes{at}vassar.edu
Received 17 March 1999; revised 19 June 2001; accepted 31 July 2001.
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ABSTRACT |
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Studies were conducted to test the hypothesis that dusky-footed wood rats (Neotoma fuscipes) place bay leaves (Umbellularia californica) on or near the sleeping nest in their stickhouses, with the result that the leaves act as a fumigant against nest-borne ectoparasites. Although many stickhouses were found to contain bay, oak, and toyon leaves, only bay was found significantly more often near the nest than away from the nest. Bay leaves were nibbled in a fashion consistent with the release of fumigating volatiles. Oak leaves, a known food staple, were nibbled in a fashion more consistent with eating. Analysis of the density of ectoparasites in samples of sleeping nest material showed few parasites in most nests, but heavy infestations in a few nests revealed the potential for large numbers of nest-borne ectoparasites. Samples of 1 g of whole and torn leaves of bay, toyon, and oak were incubated with flea larvae in mason jars for 72 h. Torn leaves (to simulate nibbling effects) of bay significantly reduced larval survival to 26% compared to 87-94% survival of larvae incubated with torn oak and toyon leaves. These findings provide evidence that dusky-footed wood rats place bay foliage around the sleeping nest with the effect of reducing their exposure to nest-borne ectoparasites.
Key words: antiparasite behavior, ectoparasites, Neotoma fuscipes, nest fumigation, plant volatiles, Umbellularia californica, wood rats.
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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There is increasing evidence that ectoparasites can produce fitness costs in hosts, presumably resulting in selection for defensive behaviors against parasites (Hart, 1990
,
1992;
Lehman, 1993). Rodents that
dwell in nests or burrows are particularly susceptible to the buildup of
nest-borne ectoparasites because the microclimate of occupied burrows provides
a dark, moist, and warm environment, and the year-round presence of the host
provides a regular food supply. In addition to grooming, one way of dealing
with the threat of nest-borne parasites is to change nest sites, a practice
not uncommon in birds (Duffy,
1983; Hart, 1997;
Møller, 1990). If an
animal can continue to use an old nest, the costs of changing nest sites
should be avoided, provided the excessive buildup of ectoparasites can be
prevented.
One type of nest protection against ectoparasites in avian species is the
use of certain volatile-producing plants woven into the nest matrix. The nest
fumigation hypothesis was initially suggested by Wimberger
(1984) and was experimentally
pursued by Clark and Mason
(1985,
1988) in the European starling
(Sturnus vulgaris). Starlings selected plants that released the most
volatiles, and in laboratory tests, volatiles of some plants suppressed the
hatching of louse eggs and the development of mites. Plants produce these
volatile products to protect against insect herbivores
(Langenheim, 1994;
Swain, 1977) and pathogenic
microorganisms (Deans and Ritchie,
1987; Knobloch et al.,
1989).
Exploring the nest fumigation hypothesis in burrowing mammals would be
difficult because of the inaccessibility of the nests. Wood rats construct
above-ground stickhouses with accessible sleeping nests. Previous
investigators (Linsdale and Tevis,
1951; Vestal,
1938) have noted that the folivorous, dusky-footed wood rat
(Neotoma fuscipes) brings fresh, green foliage into its stickhouse.
The presence of foliage in stickhouses has been interpreted as food storage,
and the typical foods of N. fuscipes, which include oak foliage
(Quercus spp; Atsatt and Ingram,
1983), were common in the houses that we inspected in preliminary
observations. Our preliminary observations also revealed that California bay
(laurel; Umbellularia californica) was present in many stickhouses in
relatively large quantities. This was of interest because N. fuscipes
is believed not to use bay foliage as a food staple; it eats only blossoms of
bay (Cranford, 1977;
Linsdale and Tevis, 1951). Our
preliminary observations also revealed that rats typically nibble on bay and
on toyon (Heteromeles arbutifolia), another frequently found plant,
as well as on oak leaves.
California bay has a high monoterpenoid content, which is noted for its
biocidal activity; correspondingly, bay exhibits little evidence of insect
herbivory or disease (Fowells,
1965). The major constituents of volatile oils in the foliage of
California bay are 1,8-cineole (19%), which is primarily responsible for the
leaves' distinctive odor, and umbellulone (39%), which has been shown to be
toxic when fed to laboratory mice (Buttery
et al., 1974; MacGregor et
al., 1974). Bay leaves are reputed to be effective in repelling
fleas from humans and human dwellings
(Balls, 1962;
Chestnut, 1902), so their
presence in stickhouses raises the question of the possible use of bay foliage
as a fumigant to control one or more developmental stages of
ectoparasites.
There were three aspects to this study. The first dealt with a quantitative description of the location and turnover of leaves within the nest, as well as the pattern of nibbling on bay compared with nibbling on oak and toyon leaves. The second aspect was an analysis of the nest matrix from wood rat houses for types and numbers of ectoparasites. Third, because fleas are known to infest adult wood rats and were usually found in samples of sleeping nest material, an experiment was designed to test the comparative effectiveness of volatiles from bay, oak, and toyon on killing flea larvae.
Study species
Dusky-footed wood rats, or packrats as they are often called, construct
durable, above-ground stickhouses using available twigs and woody debris from
the forest floor. These stickhouses offer protection from the weather and
predators. Because of the ever-present threat of predators
(Verts and Carraway, 1998),
wood rats remain in their stickhouses except for nocturnal excursions for
foraging and bringing sprigs of foliage and building materials back to their
houses (Vestal, 1938).
Radiotelemetry and live-trapping data suggest that wood rats occupy the same
stickhouse for several months at a time
(Cranford, 1977;
Wallen, 1982). Linsdale and
Tevis (1951) reported that
stickhouses are occupied serially generation after generation and may last a
decade or longer. This pattern of stickhouse reuse would suggest a risk of
ectoparasite buildup.
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METHODS |
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Study site
The study population was located in Sonoma County, northern California, USA, in a mixed hardwood forest of 80 ha. The forest was located on a predominantly north-facing slope with elevations of 60-150 m above sea level. Most numerous among the trees which made up the closed canopy were California bay, coast live oak (Q. agrifolia), and interior live oak (Q. wislizenii). Much less numerous among the trees were Douglas fir (Pseudotsuga menziesii) and madrone (Arbutus menziesii). Common woody plants in the understory were toyon, California hazel (Corylus cornuta), and poison oak (Rhus diversiloba). The herbaceous layer was dominated by sword fern (Polystichum munitum), miner's lettuce (Monitia perfoliata), cow parsnip (Heracleum lanatum), and false Solomon's seal (Smilacina racemosa).
Observations at our study site revealed that stickhouses were nonrandomly
distributed in the forest and were found where oak stood alone or where it
intermingled with other trees, especially bay and/or toyon. Areas without oak
trees contained no stickhouses. Nearly all of the stickhouses were on the
ground; the few that were located in the tree canopy (estimated at less than
5%) were not studied. Houses were 1.0-1.5 m in height and 1.5-2.5 m diam at
the base and were constructed of decaying sticks and fragments of bark. Some
had fronds (fresh and/ or dried) of sword fern woven into the structure.
Approximately half of the houses were constructed next to, or among, diverging
trunks of bay or oak trees; others were free standing or enclosed within
poison oak shrubbery. Individual leaves and sprigs of fresh foliage were
regularly found throughout the interior of the stickhouses. Sleeping nests
were constructed of lichens, mosses, dried grasses, and shredded bark and wood
and varied considerably in mass (30-215 g). Nests contain a pocket
approximately 8 cm diam. The arrangement, size, and number of chambers and
tunnels within stickhouses were variable and similar to that described by
previous investigators (Linsdale and
Tevis, 1951).
Location, turnover, and pattern of nibbling on leaves
If bay foliage were used by wood rats to control nest-borne ectoparasites,
one would predict that this foliage would be found disproportionately near the
sleeping nest, compared to other species of foliage used as food. Bay would
also be frequently replaced in order to keep levels of volatiles high.
Further, because of the containment of volatiles within secretory idioblasts
scattered through the bay leaf
(Klasapligil, 1951), volatiles
would be released more readily if the leaf were cut or broken open by sporadic
nibbling. Although rats might nibble on both food staples and bay, the pattern
of nibbling should be different between bay and food staples such as oak
leaves. A leaf partially consumed as food would be expected to be missing
substantial amounts of tissue at one end or from margin to central vein,
whereas a leaf damaged to increase release of volatiles would be expected to
exhibit torn tissue without much tissue missing. These predictions were
explored in this study conducted during the months of June—August 1994
(year 1) and 1995 (year 2).
We inspected chambers through an entrance tunnel with a videostick (a small CCD video camera mounted on the end of an articulating wand; RJ Electronics, Salem, Oregon) introduced through an existing tunnel entrance or a small hole on one side of the stickhouse. In 1994, 34 marked stickhouses were examined to determine the location of foliage types within the chambers. In 1995, 16 additional houses not observed in 1994 were examined to extend the sample. For the purposes of analysis, the two species of oak were combined. The areas within each stickhouse were designated as "near the nest" and "non-nest areas"; leaves located on the rim of the sleeping nest or within 5 cm of the sleeping nest were referred to as "near the nest."
We measured turnover of foliage in 1995. Nine houses were each inspected five times at intervals of 2-3 days over a period of 2 weeks. At the time of each inspection, all foliage was removed from the house after noting the location of each item. Individual leaves were distinctively marked with a paper punch and the foliage was then replaced in the same location from which it had been removed. For each reinspection it was possible to assess how much of the foliage present had been added since the previous inspection and thus calculate the proportion of the total foliage that was new. For each house we used the average of these proportions as the estimate of turnover of each plant type.
In 1994, we measured the percentage of houses in which nibbling was observed on any of the three plant types for the 34 stickhouses. We also recorded the pattern of nibbling on each plant species, differentiating between that expected to apply to eating versus that for the release of volatiles.
Ectoparasites in the sleeping nests
We evaluated ectoparasites in sleeping nests in the summers of 1995 (year
2), 1997 (year 4), and 1998 (year 5), inspecting 11, 7, and 10 different
nests, respectively, in these years. Complete nests were removed through a
small hole in the wall of each stickhouse. The nesting material was
immediately placed in a deep plastic bowl, weighed, and then mixed in an
attempt to evenly distribute ectoparasites before sampling. A sample of 20-30
g of material was sealed in a plastic bag for extraction of nest-borne
ectoparasites. The remaining material was replaced in the nest chamber, and
the sticks that had been removed were replaced in the wall. This procedure
apparently had no lasting effect on the occupant because a few days later
stickhouses were found to contain fresh vegetation, and the sleeping nest's
shape had been restored.
Nest material was subjected to a modified Berlese-Tullgren extraction
(Southwood, 1978). Two
replicate 10 g samples were placed into polypropylene funnels, each containing
a 1.7-mm mesh aluminum screen floor to support the sample and each covered
with elasticized nylon cloth to prevent escape of ectoparasites. Each funnel
was placed 7 cm beneath a 50-W floodlight for 2 days to drive adults and
immature forms of ectoparasites from the nest material into the funnel. The
spout of each funnel led to a collection tube containing 5 ml of 80% ethyl
alcohol preservative. Preserved material in the tube was later passed through
filter paper so that we could identify and count ectoparasites. Preliminary
trials indicated that no live mobile ectoparasites remained in the nest
material after 48 h. We counted mature fleas, flea larvae, and ticks (larval
and nymphal stages combined) under a dissecting microscope. Estimated numbers
of ectoparasites in the entire nest were calculated on the basis of
extrapolation from the proportional weight of the nest samples evaluated. Two
genera of fleas (Orchopeas sp. and Anomiopsyllus sp.)
parasitize wood rats (Lindsdale and Davis,
1958). For the purposes of this study, adult and larval fleas of
both species were combined.
Effects of leaf volatiles on flea larvae
We used cat fleas (Ctenocephalides felis) in this experiment
because this is the only species readily available in large numbers. Larvae,
rather than eggs or adults, were chosen for the assay because larvae have a
soft integument compared to the possibly more protective capsule of eggs and
exoskeleton of adults and because larval growth extends over a period of 8-10
days before pupation (Silverman et al.,
1981). In nature, larvae in the nest would be exposed to volatiles
over this 8- to 10-day period. We tested equal quantities of whole and torn
leaves of each of the three plant species regularly found in the stickhouses.
Tearing of the leaves was intended to simulate nibbling and increase the
release of volatiles.
The experiment (conducted May—June 2000) tested whole and torn leaves from 10 bay trees, 10 oak trees, and 10 toyon trees at our research site. All 30 trees sampled were located in areas with active wood rat stickhouses nearby. The sprigs selected from each tree showed no visible signs of disease. We collected sprigs at 1100-1700 h, placed them in plastic bags, and refrigerated the bags within 2 h of harvest. Cat flea eggs from a commercial supplier (El Lab, Soquel, CA) were collected 24 h after oviposition and arrived in our laboratory the next morning. Eggs were placed in an incubator at 24-26°C with relative humidity maintained at 75-80%. Hatching of eggs into larvae was complete 4 days after their collection by the supplier, at which time we exposed the larvae to the leaves.
Exposure of larvae to leaves occurred in sealed 1-quart mason jars. Each jar lay on its side and contained a 12 x 5 x 3 cm high plastic tray, which held a heap of 80 g of NaCl and 50 g of saturated NaCl solution. This kept the relative humidity inside the jar, once sealed, between 75-80%, countering the tendency of transpiration of the leaves to raise it above optimal level. On the top of the tray was hardware cloth fashioned to remain securely in place and to provide a stable setting for a 60 x 15 mm petri dish containing larvae. Larvae, along with particles of larval food (feces of adult fleas fed blood in a membrane culturing technique), were sprinkled into each dish until the number of larvae was between 20 and 30, the exact number of larvae being recorded for each dish. A piece of 1.7-mm mesh aluminum screen was placed above the dish with larvae, and it was on this screen that 1 g of torn or whole leaves was placed just before the jar was sealed. We used 12 mason jars in assessing each tree; five contained whole leaves, five contained torn leaves, and two contained no foliage and served as controls. Thus each foliage sample was tested with 100-150 larvae. Mason jars were placed in incubators to control temperature between 24° and 27°C. We counted the number of live larvae in the five dishes 3 days later. We determined the total number of larvae that had survived for each plant species under both torn- and whole-leaf conditions on each trial and compared this number to the number originally present. Whole and torn leaves for each plant species were from the same branch, and tearing created leaf fragments 1-2 cm wide. Previous experience with this system revealed that on rare occasions the water content of the foliage sample surpassed the capacity of the salt to regulate the relative humidity, resulting in the larval food particles liquifying, entrapping, and suffocating larvae and invalidating the results of that dish. If this occurred in more than two of the five dishes being used to assess a foliage sample, we eliminated data from that tree from the analysis.
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RESULTS |
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Location, turnover, and pattern of nibbling on leaves
Almost all houses contained fresh leaves of one or more of the four species of interest—California bay, interior live oak, coast live oak, and toyon. Poison oak, false Solomon seal, cow parsnip, and miner's lettuce were found infrequently. Toyon usually was found as individual leaves, whereas oak and bay were most often found as sprigs. As illustrated in Figure 1, foliage of bay was found in 72% of the 50 houses, compared to about 30% for toyon and oak. This difference in the occurrence of bay in stickhouses in comparison with toyon and oak was significant (
2 = 14.24, df = 2, p
<.001). Of those houses where foliage of each plant species was found,
Figure 1 also shows that bay
was much more likely to be found near the nest than toyon or oak
(2 = 8.78, df = 2, p <.02) and much less likely to
be found in non-nest areas than toyon or oak (2 = 8.60, df =
2, p <.02).
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Bay was nibbled in 43% of houses in which it was found; for toyon and oak the values were 80% and 75%, respectively. Chi-square analysis indicated that differences in the occurrence of nibbling seen in bay, oak, and toyon were not statistically significant. The pattern of nibbling on oak and toyon leaves was of the sort expected for food items, but the pattern of nibbling on bay was not, consisting of individual shallow bites around the margin of the leaf with little tissue removed. Replacement of oak, toyon, and bay foliage within stickhouses was frequent, with a mean turnover of 80% (n = 9), 78% (n = 9), and 68% (n = 9) for oak, toyon, and bay, respectively.
Ectoparasites in the sleeping nest
Agreement between the two 10-g replicates of each of 28 nests was
significant for the flea larvae (Spearman correlation coefficient, r
=.56, p <.05) and adult fleas, (r =.68, p
<.05), but not ticks (r =.39). Estimates of the number of
ectoparasites in the nest were calculated using the mean of the two
replicates. Ectoparasite numbers varied considerably between years and among
stickhouses within a year (Table
1). Median numbers of ectoparasites were lower in 1997 than in the
other 2 years. The numbers of parasites at the upper ends of the reported
ranges (e.g., 601 ticks; 223 flea larvae) indicate that heavy infestations in
the sleeping nest are sometimes realized.
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Effects of leaf volatiles on flea larvae
The results of incubating flea larvae with exposure to either torn or whole
leaves of each plant species is illustrated in
Figure 2. Data from one oak and
one toyon were eliminated because of liquification of larval food particles in
three of five dishes; thus sample sizes for bay, toyon, and oak are 10, 9, and
9, respectively. A two-way ANOVA conducted on arcsine-transformed data
revealed significant factor effects for species (F = 29.37, df = 2,
50; p <.0001) and leaf condition (F = 51.65, df = 1, 50;
p <.0001) and a significant interaction between factors
(F = 31.54, df = 2, 50; p <.0001). Inspection of
Figure 2 indicates that torn
bay leaves with a survival of 26.4% were responsible for the significant
factor and interaction effects. Mean survival rates for other leaf types
ranged from 87.6 to 94.4%. Mean survival rate for jars containing no foliage
(n = 60) was 94.9%.
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMETHODSRESULTSDISCUSSIONREFERENCES |
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Wood rat nests, like those of other rodents, harbor ectoparasites. Examination of the ectoparasite density of the sleeping nest matrix revealed that the majority of wood rat nests contained developmental stages of fleas and ticks. Although considerable variability in numbers of ectoparasites was found between individual sleeping nests and between years (some nests with few and some with large numbers of parasites), the potential clearly exists for a major buildup of ectoparasites. It is possible that, in spite of the swiftness and care with which nest material was sampled, the methodology underestimated the numbers of parasites present. Disturbance of the nest may have caused adult fleas or larvae of ticks and fleas to move away, or parasites may have dropped out of the nest when it was removed from the stickhouse. Additionally, the extraction procedure may have killed some mobile parasites that remained in the nest matrix.
If the methodology did reveal a good estimate, then the relatively few ectoparasites found in many nests suggests that the parasite defense behaviors of wood rats may be effective in controlling the number of parasites. The use of bay leaves on or near the nest was the parasite defensive behavior addressed in the present study. Bay leaves are known to produce volatiles toxic to ectoparasites. Our observation of the placement of bay leaves in disproportionate proximity to the sleeping nests, compared with bay placement in other parts of the stickhouse, stands in contrast to no indication for selective placement of toyon and oak near the sleeping nest and is consistent with the role of bay being used as a fumigant against nest-borne ectoparasites.
There was a substantial turnover of bay leaves within 2-3 days, a behavior which could maintain concentration of released volatiles. The pattern of nibbling on bay leaves, typically as small lacerations sporadically along the margin of the leaf, was not suggestive of use of bay for food but did suggest a function in releasing volatiles. The nibbling of oak, a known food staple (see below), involved removal of large sections of the leaf, as would be associated with eating. Whether wood rats eat any small parts of bay leaf that are removed is not clear.
The most convincing finding in favor of the nest fumigation hypothesis was the experiment on incubation of bay, toyon, and oak leaves with flea larvae. In this experiment, in which leaves of all three species were torn to simulate nibbling (and facilitate the release of biocidal volatiles), torn bay significantly reduced survival of flea larvae to 26.4%, compared with the 87.6-94.4% survival seen after incubation with torn oak leaves, torn toyon leaves, or control. Incubation with whole bay, toyon, or oak did not reduce survival of larvae compared with control. Nest fumigation, as a behavior that reduces nest-borne ectoparasites, provides a means by which the wood rats may continue to occupy a house for several seasons, a well-known phenomenon. Flea larvae may forage on plant debris in the nest, so it is possible that if nest-borne larvae consume old, decaying fragments of bay leaves, this may also kill some larvae. We did not test this possibility.
With regard to the presence of oak leaves in the stickhouses, it is well known that oak is used as food and is cached in the stickhouses. In laboratory studies, the dusky-footed wood rat has been shown to thrive on oak and acorns in spite of its high tannin content (Attsatt and Ingram, 1983), and our findings support the use of oak as a food staple. Oak was replaced every 2-3 days, and we found clear signs of oak leaves being eaten (in a different fashion than the nibbling on bay). The frequent finding of toyon leaves in stickhouses is not readily explained because the plant has not been studied as a food staple, and yet there was no evidence of it being toxic to flea larvae.
The prospect of the use of bay by wood rats for nest fumigation raises a
number of compelling questions. One is whether the use of plants by
preparturient and post-parturient female rats with pups may differ from that
of males. Another question is the degree to which such use of plants for
defense against nest-borne ectoparasites may be characteristic of other
species of wood rats that live in different geographical areas with different
plants available to them. Of interest in this regard is the presence of plant
species of the genera Juniperus and Artemesia in the den
sites of N. cinerea (Smith,
1997). Some junipers are reputed to be effective in the control of
fleas and mites (Huddle,
1936), and some members of the genus Artemesia are
effective against ixodid ticks (Jacobson,
1975). A related question is the degree to which burrowing rodents
or lagomorphs might also use plants with fumigating properties. Finally, if
the nest fumigation hypothesis is true, there is a question of whether bay may
be used regularly on a prophylactic basis or whether the wood rats, sensing a
buildup of nest-borne ectoparasites, elect to use plants at the most
appropriate times.
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ACKNOWLEDGEMENTS |
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We thank Peter Connors for assistance in identifying plants; students R. Lewisen, C. Camburn, J. Stander, D. Dau, A. Allen, B. Sinwell, C. O'Brien, A. Avnayim, B. Johns, V. Leytin, D. Hansen, and B. Selgado for assistance; staff research associate Kelly Cliff for technical assistance; and landowners Joe and Kathy Tresch for access to the study site. This research was supported in part by grant IBN-96-17407 from the National Science Foundation and in part by the Class of 1942 Fund for Research in Environmental Sciences at Vassar College.
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