Evidence for Coevolution between Mammalian Herbivores and Plant Secondary
Compounds in Boreal Forests
Troy Gerhardt
April 24, 1994
Colorado State University
Fort Collins, Colorado 80523
Introduction
Browsing mammals are generally highly selective feeders, consuming
only a small portion of the plant species and plant parts available to
them. The basis for this selectivity remains relatively unknown,
despite attempts to explain diet selection in terms of nutrients or
energy (Bryant and Kuropat 1980, Palo and Robbins 1991). Recently, the
importance of plant secondary compounds as determinants of browsing
patterns has been recognized (Palo and Robbins 1991). Such chemically
mediated interactions between mammalian herbivores and woody plants may
lead to evolutionary responses in both the browsers and the food plants.
A major evolutionary response of plants to herbivory has been a
production and diversification of secondary compounds that deter
feeding.
Browser-plant interactions in boreal regions are of interest
because of the combination of often intense herbivory by several
mammalian species and because of the relatively low temperatures, light
levels, and nutrient levels under which boreal plants grow. Also, in
these systems, the effects of secondary compounds in a variety of plant
species have been proposed to expand beyond bite selection by individual
browsers to influence community and ecosystem properties (Bryant 1987,
Bryant et al. 1991a, Tahvanainen et al. 1991, Bryant et al. 1992, Molvar
et al. 1993). Bryant and Kuropat (1980) reviewed the plant
characteristics that affected the winter foraging patterns of boreal
vertebrates and suggested that because boreal forests are taxonomically
monotonous, secondary compound diversity would also be relatively low.
Still, they concluded that vertebrate browsing patterns were strongly
influenced by secondary compounds, and more recent studies have
succeeded in determining the distribution and effects of specific
compounds on the feeding patterns of hares, moose and voles browsing on
boreal plants.
This review will consider the potential for coevolutionary
interactions between plant secondary compounds and browsing mammals in a
relatively simple system. I will first briefly present several
theoretical ideas on plant-animal coevolution and then present the
evidence on interactions between mammalian browsers and woody plants in
boreal regions that may bear on the coevolutionary questions.
Theoretical coevolution
Definitions of coevolution
Coevolution between plant defenses and the herbivores that feed on
them has been discussed at multiple scales. Trends of variable chemical
deterrence are noticeable within the plant kingdom as a whole, with the
complexity of secondary compounds generally increasing from ferns
through herbaceous angiosperms (Harborne 1988). Within plant families,
trends of increasingly complex and effective chemical deterrents are
evident (Berenbaum 1983). Additionally, several considerations of
coevolution discuss the relationship between the evolution of new
secondary compounds and adaptive radiation in both plant and herbivore
(Ehrlich and Raven 1964, Rhoades and Cates 1976).
Reciprocal adaptations between plant defense and herbivore
browsing can occur at more restricted scales. In a simplified case,
genes that result in plant secondary compounds that deter herbivory will
spread through the plant population if selective forces from herbivory
are strong. Herbivores will be prevented from feeding on the plants or
will suffer ill effects when they do feed on the defended plants until
they evolve means to handle these chemicals. If selective forces favor
this adaptation, the ability to feed on plants containing the deterrent
compound will spread through the herbivore population, and the plant is
again unprotected from these herbivores.
Criteria for documenting coevolution
The likelihood and documentation of such evolutionary interactions
depend on the existence of several conditions.
1) Plants show intraspecific variation in the amount of herbivore
damage (Marquis 1992).
2) Variability in damage correlates with the presence or
concentration of a secondary compound or compounds (Marquis 1992).
3) Damage correlates with fitness (Marquis 1992).
4) Plants show additive genetic variance for the production of the
compound, and thus for damage (Marquis 1992).
5) Herbivores have intraspecific variation in their ability to
handle secondary compounds.
6) The ability to handle the compound shows additive genetic
variance.
7) The ability to handle the compound correlates with fitness.
Demonstration of these and the micro-evolutionary processes leading
to reciprocal adaptations has not been done in a natural system. Most
studies document, or attempt to document, only a few of these
conditions. For most studies, correlations of damage with plant fitness
are lacking (Endler 1986), and the importance of herbivory as a
selective force is questioned repeatedly (Marquis 1992). Thus to
evaluate coevolution in natural systems requires the use of the
available evidence that applies to the listed requirements as well as
indirect evidence.
Browsers and food plants in the boreal forest
The vegetation of resource-limited areas such as the boreal region
is characterized and dominated by slow growing, woody plants that are
relatively poor food for mammals (Bryant et al. 1991). The diversity of
plant species is low: species such as the deciduous willows (Salix
spp.), birch (Betula spp.), alder (Alnus spp.), and poplar (Populus
spp.) and the evergreen Scots pine (Pinus sylvestris) often form
monospecific stands.
Three main groups of mammalian herbivores in these forests are
rodents (voles and lemmings), hares (Lepus spp.) and cervids (moose,
Alces alces; Tahvanainen et al. 1991). All feed on woody plants but
because of body size and dental differences, select different portions
of plants. Browsing by all three groups is particularly heavy in the
winter months and at the peaks of hare or rodent population cycles.
Variation in secondary compounds and browsing resistance
Variation in secondary compounds: potential for defense
Substantial variation in secondary compounds exists among
congeneric plant species and within distinct populations of a single
species (Bryant et al. 1989, Rousi et al. 1991). Experiments on birch
and willow found that genetic differences do exist, a necessary
condition for coevolution in these systems.
Families of birch seedlings (B. pendula) from Finland and Siberia
and crosses between these families differed in the amounts of
papyriferic acid-containing resin on their bark (Rousi et al. 1993).
All trees were grown from seed in a greenhouse to control for phenotypic
responses to variable environmental conditions. Individuals of B.
pendula, B. platyphylla, and B.pendula x B. platyphylla hybrids raised
in a similar environment showed significant differences in the amount of
resin produced (Rousi et al. 1991). B. platyphylla (originating from
eastern Asia, and often considered a subspecies of B. pendula) showed
particularly large amounts of resin and thus secondary compounds.
Frequency distributions of number of resin droplets within families and
crosses were consistently unimodal, suggesting additive genetic
variation for defense compounds (Rousi et al. 1991). Experiments on
other boreal plants such as willow (Bryant et al. 1989, Nichols-Orians
et al. 1993, Danell pers comm) and Scots pine (Rousi 1989) have found
similar variation in defense compounds between families and genotypes.
Variation in browsing resistance and correlations with secondary
compound production
The potential for coevolution involving secondary compounds depends
on a correlation between the production or concentrations of secondary
compounds and the level of browsing damage. For the studies discussed
above, this relationship was strong. Among B. pendula families and B.
pendula x B. platyphylla hybrids, resin content was inversely related
to mountain hare (Lepus timidus) preference (Rousi et al. 1991). Resin
levels of B. platyphylla were approximately twice as high as those in
any other family or cross, and browsing damage was about one third the
average for other families (Rousi et al. 1991). In a separate study,
variation in both vole (Microtus agrestis) and hare (L. timidus)
browsing on different genetic lines of birch (B. pendula) was correlated
with levels of secondary compounds (Rousi et al. 1993).
Other studies have shown similarly strong correlations between
levels of mammalian browsing and levels of specific secondary compounds
in boreal plants. Levels of papyriferic acid in birch (Reichardt et
al. 1984), salicaldehyde, 6-hydroxycyclohexenone, and 1,2-
cyclohexadione in balsam poplar (Populus balsamifera; Reichardt et al.
1990, Clausen et al. 1992), pinosylvin and pinosylvin methyl ether in
green alder (Alnus crispa; Clausen et al. 1986) and the phenolic
glycosides salicortin, picein, salidroside and acetyl salicortins in
willow (Salix spp.; Tahvanainen et al. 1985) have all been shown to
regulate the preference of mammalian browsers for plants.
In most of these studies, the genetic variation among plants was
either not known, not measured, or not reported. However, any
demonstration that secondary compounds correlate with herbivore
preference, and therefore relative broswing damage, is relevant to
coevolutionary questions. The distribution of secondary compounds
within a plant (Palo 1984) and between adult and juvenile forms of the
same plant (Bryant et al. 1991a,b) is not uniform and browsing is
directed towards those parts that are least defended (see reviews in
Bryant et al. 1991 a,b, Tahvanainen et al. 1991). In the past decade,
most studies on variability in defense and resistance have focused on
phenotypic variation due to environmental conditions rather than genetic
differences (Bryant et al. 1983, 1987, Waring et al. 1985, Reichardt et
al. 1991). Thus, although few studies document both genetic variation
in chemistry and resistance, there is strong evidence that browsers
discriminate based on levels and types of secondary compounds as well as
evidence that secondary chemistry is at least partially genetically
determined.
Estimating plant fitness
Determining the correlation between chemistry, damage and plant fitness
As mentioned earlier, the relationship between the amount of
herbivore damage and plant fitness is poorly documented and debate over
the relationship is inconclusive (Fritz and Simms 1992). Of importance
for evaluating coevolution is determining the cost of producing the
observed levels of secondary compounds in comparison to the benefits
gained from being defended against herbivores (Zangerl and Bazzaz 1992,
Simms 1992). In many cases, the ability to determine this relationship
is hindered by uncertainty about the relevant currency to measure (Simms
1992).
Although I could find no direct estimates of this relationship for
boreal systems, several lines of indirect evidence may be used to
evaluate this chemistry-damage-fitness relationship. In terms of
fitness, the value of different plant parts varies. Similarly, the
value of a plant part likely changes depending on the stage of plant
development. Studies on boreal plants have been exceptionally detailed
in measuring the variation in secondary chemistry between plant parts
and between different developmental stages (Palo 1984, Bryant et al.
1991a,b). The available evidence suggests that juvenile plants are
generally more defended and less palatable to browsers than adult plants
(Bryant et al. 1991a,b, Tahvanainen et al. 1991). Intra-plant variation
also exists within a single season: the upper branches of adult trees
are beyond the reach of even moose and generally have significantly
lower levels of secondary compounds. When offered to herbivores along
with lower branches in the juvenile stage or branches from juvenile
plants, these less defended branches are preferred (Bryant et al.
1991b). Additionally, boreal plants tend to have higher concentrations
of secondary compounds in winter, the time of the most intense browsing
(Palo 1984). These observations all suggest that plant production of
secondary compounds is related to the levels of browsing on those plant
parts and to the fitness value of different plant parts.
Biogeographic evidence
Biogeographic studies provide additional indirect evidence on the
fitness value of deterrence provided by secondary compounds. Because
past selection is difficult to verify, geographic patterns of secondary
compound variation are difficult to interpret. However, the available
evidence at these large scales does correlate with the estimated
importance of browsing as a selective force.
Bryant et al. (1989) reported biogeographic differences in
secondary compounds for birch and willow. They compared the levels of
various secondary compounds in several species and populations of birch
and willow and correlated chemical differences to browsing by two
species of hares. Both levels of secondary compounds and resistance to
browsing hares varied across geographic regions. For Finnish mountain
hares (Lepus timidus) birch grown in a common garden decreased in
palatability from Iceland (Betula pubescens), to Finland (B. pendula, B.
pubescens, B. nana) to Siberia (B. middendorffii). Concentrations of
secondary compounds (papyriferic acid and 3-0-malonylbetulafolientriol
oxide I) also varied and were inversely correlated with hare preference.
For Alaskan snowshoe hares (L. americanus), preference was again
inversely correlated with concentrations of secondary compounds and
decreased from Finnish birch (B. pendula and B. pubescens) to Alaskan
birch (B. nana and B. resinifera). With willow twigs, both snowshoe and
mountain hares preferred willows from Finland (Salix caprea and S.
phylicifolia), which showed lower levels of several phenolic glycosides
(salicortin, picein, salidroside, and acetyl salicortins; Tahvanainen et
al. 1985), than those from Alaska (S. alaxensis and S. arbusculoides).
Both the concentrations of defensive compounds and the palatability
of different plants were related to the level of browsing history found
in the habitat from which the plants were collected (Bryant et al.
1989). Iceland had no browsing mammals before Norse colonization and
plants there still experience relatively low levels of browsing. In
contrast, Alaskan and Siberian plants experience much higher levels of
herbivory, due in part to the especially intense browsing during the
peak of the 10-year hare population cycles. Additionally, both Alaska
and Siberia supported a large and diverse browsing fauna throughout the
Pleistocene (Bryant et al. 1989). Although this study did not directly
measure fitness, it does imply that differences in plant defense are
correlated with levels of browsing, and thus that in areas that
experience heavy browsing, fitness is improved by producing chemicals
that deter browsers.
The herbivores: hares, moose, and voles
Genetic variation and additive variance
In contrast to the plants, the herbivores' side of any potential
coevolutionary interaction in boreal systems is relatively unexplored.
Because many estimates of browsing use wild animals, measurements of
intraspecific variation in the ability to deal with secondary compounds
are lacking. The design of these studies also precludes determining
whether any variation between individual browsers is genetically
determined.
Studies of congeneric hares (Lepus spp.) have shown differences in
willingness to ingest secondary compounds and differences in the effects
of specific compounds. Alaskan snowshoe hares (L. americanus) and
Finnish mountain hares (L. timidus) showed similar preferences for
willow and birch twigs that differed in their levels of secondary
compounds (Bryant et al. 1989). However, unlike snowshoe hares,
mountain hares refused to eat the most heavily defended plants at all.
Birch and willow from geographic regions that were most intensely
browsed had higher levels of secondary compounds and were avoided by
mountain hares even when no other forage was offered. This suggests
that snowshoe hares, which inhabit regions where plants are relatively
heavily defended, can eat greater masses of secondary compounds than
Finnish mountain hares. Bryant et al. (1989) propose that this
difference is a result of better detoxification mechanisms in snowshoe
hares, and if so, chemical coevolution has occurred.
Similar differences were found between mountain hares and European
hares (L. europaeus) feeding on diets containing extracts of birch (B.
pendula) secondary compounds. European hares typically feed on grasses
instead of woody plants; mountain hares feed heavily on birch. Birch
secondary compounds are known to cause sodium imbalances and reduced
digestibility of dry matter and protein in hares (Iason and Palo 1991).
In both hare species, the birch extract decreased digestibility by
approximately similar amounts. However, sodium balance in mountain
hares was unaffected by increasing levels of extract (up to 80% that
found in live birch twigs) while that of European hares decreased
severely with increasing levels of extract suggesting a lower tolerance
for birch secondary compounds (Iason and Palo 1991). Together these
studies provide evidence that at least between species, the ability to
deal with specific secondary compounds varies. The differences in
abilities to ingest or detoxify high levels of secondary compounds was
correlated with the importance of foods containing these compounds in
the hares' natural diet.
Correlation between diet and fitness
The evidence for the effects of secondary compounds on fitness has
not been measured directly for boreal mammals. However, the evidence
presented above suggests that they may be important. Both the fine-
scale selectivity of browsers among similar plants and plant parts that
vary in their levels of secondary compounds (Bryant et al. 1991a,b,
Bryant et al. 1992) and the potentially severe effects of these
chemicals on the herbivores' nutritional status (Iason and Palo 1991)
suggest that the ability to avoid or detoxify secondary compounds is a
result of selection.
Conclusion
Most studies on boreal browsing systems involve either moose,
hares, or voles. Studies on the chemical aspects of other boreal
mammal- (reindeer/caribou, white-tailed and Sitka deer, roe deer,
lemmings) plant interactions are scarce. Moose, hares, and vole
preferences are generally well correlated (Bryant and Kuropat 1980,
Tahvanainen et al. 1991, Bryant et al. 1991a), suggesting that they may
exert similar selective pressures on plant chemistry. However,
differences in the digestive systems of each probably result in
different fitness consequences for feeding on or avoiding different
secondary compounds. Thus, the reciprocal selective pressure of the
plants on the herbivores may be unequal. The effects of specific
secondary compounds on moose are unavailable and no comparisons have
been made between either populations or subspecies of these browsers.
Although the direction of selection on plant chemistry may be similar
among herbivores, the intensity of this selection probably varies.
Differences in body size and especially population sizes between these
herbivores would tend to influence their selective intensity since the
relative importance of food quality versus food quantity may depend on
both. The importance of the 10-year hare population cycles and
browsing by large mammals during the Pleistocene as strong selective
pressure was emphasized by Bryant et al. (1989).
The conditions necessary for coevolution have been studied to varying
degrees in the boreal system. Variation in plant secondary chemistry is
relatively well explored compared to variation in browsers abilities to
handle or avoid them. Perhaps the single best study supporting boreal
coevolution is the biogeographic study of Bryant et al. (1989) that
found differences in secondary compound levels correlated to browsing
among geographically distinct plant populations that differed in the
current and historical levels of browsing they experience. The
available evidence suggests that the observed interactions between
plants and mammalian herbivores could be the result of chemical
coevolution.
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