Popul Ecol (2010) 52:461–473
DOI 10.1007/s10144-010-0210-0
SPECIAL FEATURE: REVIEW
Trait-Mediated Indirect Interaction
The resource regulation hypothesis and positive feedback loops
in plant–herbivore interactions
Timothy Paul Craig
Received: 22 April 2009 / Accepted: 18 October 2009 / Published online: 1 May 2010
Ó The Society of Population Ecology and Springer 2010
Abstract Resource regulation occurs when herbivory
maintains or increases plant susceptibility to further
herbivory by the same species. A review of the literature
indicates it is a widespread plant–animal interaction
involving a diverse array of herbivores. At least three
mechanisms can produce this positive feedback cycle.
First, phytophagous insect and mammalian herbivore
damage can stimulate dormant buds to produce vigorous
juvenile growth, which is preferred for further attack.
Juvenilization cycles may have repeatedly evolved because
herbivores are able to take advantage of a generalized plant
compensatory response to any type of damage. Second,
herbivores can manipulate plant source–sink relationships
to attain more resources, and this alteration of plant growth
may benefit subsequent herbivore generations. Third, herbivory can alter plant nutrition or defensive chemistry in a
way that makes a plant susceptible to more herbivory.
Resource regulation probably occurs because damage to
resources preferred by the herbivores induces a generalized
plant response that produces more preferred resources.
Alternatively, manipulation of plant resources to induce
resource regulation may have evolved in herbivores with a
high degree of philopatry due to selection to alter plant
resources to benefit their offspring. Resource regulation
can stabilize insect population dynamics by maintaining a
supply of high-quality plant resources. It can also increase
the heterogeneity of host-plant resources for herbivores by
altering the physiological age structure and the distribution
of resources within plants. Resource regulation may have
T. P. Craig (&)
Department of Biology, University of Minnesota Duluth,
Duluth, MN 55812-3004, USA
e-mail: [email protected]
strong plant-mediated effects on other organisms that use
that host plant, but these effects have not yet been explored.
Keywords Compensatory growth Dormant bud Herbivory Indirect interactions Philopatry Population dynamics
Introduction
Craig et al. (1986) coined the term resource regulation to
describe a positive feedback mechanism whereby ‘‘the
maintenance or increase of high quality resources by an
herbivore that impacts immediately subsequent generations
of the same herbivore species on the same individual
plant’’. It is an induced response, which is defined by
Karban and Baldwin (1999) as any plastic responses by
plants to damage or stress from any source. Karban and
Baldwin (1999) term any such responses that have a negative impact on herbivore fitness as induced resistance,
which produces negative feedback loops. Plant responses
that increase herbivore fitness are termed induced susceptibility, which produces positive feedback loops. Using this
terminology, resource regulation is a specific kind of
induced plant susceptibility to herbivores. It is important to
note several assumptions that are not made about induced
responses (Karban and Baldwin 1999). First, it is not
assumed that there is a correlation between herbivore fitness and plant fitness as the result of induced responses.
For example, induced susceptibility that has a positive
effect on herbivore fitness can have a neutral, positive, or
negative impact on plant fitness. Second, it should not be
assumed that the induced plant responses have evolved as
the result of selection by the herbivore: the plant responses
could have evolved in response to very different selective
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pressures and herbivory incidentally induced the response
(Karban and Baldwin 1999).
Resource regulation differs from other types of induced
susceptibility in that ‘‘it impacts immediately subsequent
generations of the same herbivore species on the same
individual plant’’, whereas induced susceptibility can
influence the same generation of the herbivore, and many
of the examples cited by Karban and Baldwin (1999) fall
into this category. An unresolved question is whether the
offspring of individuals that induced the plant response
benefit from that response. If this is the case, then there
could be selection for the herbivore to alter its attack to
increase the induced plant response. Alternatively, if the
herbivore population as a whole benefited, but not the
offspring of individuals who induced the damage, then
resource regulation would be produced as an incidental
result of herbivory. In either case, the ecological effects on
insect and plant populations would be the same.
Resource regulation is a plant-mediated, indirect interaction in which individuals separated in space and time
interact with each other via alteration of host-plant traits.
Indirect plant-mediated interactions have important ecological and evolutionary effects that have only recently
been recognized (Ohgushi 2005; Ohgushi et al. 2007).
Most of the documented plant-mediated indirect interactions are among species (Ohgushi 2005), but intraspecific
plant-mediated indirect interactions may also be important
and influence interspecific interactions (Craig et al. 2007).
In this review I examine the occurrence and potential
importance of resource regulation. First, I review three
different mechanisms by which resource regulation may
occur: (1) Juvenilization as proposed by Craig et al. (1986)
whereby herbivory induces dormant bud growth, which
increases resources for the herbivore. (2) Resource
manipulation whereby herbivore manipulation of source–
sink relations increases resources for the herbivore. (3)
Nutritional or chemical alteration whereby herbivory alters
the nutritional or chemical composition of the plant that
benefits later generations without inducing dormant buds.
Next, I explore the implications of resource regulation for
population dynamics. Finally, I discuss the evolution of
resource regulation in plant–herbivore interactions.
Resource regulation through juvenilization
Craig et al. (1986) showed that Euura lasiolepis, a sawfly
(Hymenoptera: Tenthredinidae) that induces galls on the
arroyo willow, Salix lasiolepis, can maintain or increase
the population density of future generations of the galler
through their impact on willow growth (Fig. 1). Euura
lasiolepis have a strong preference for rapidly growing
shoots and high survival on those shoots. The formation of
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Fig. 1 Resource regulation hypothesis (modified from Craig et al.
1986). The galling sawfly Euura lasiolepis can create a resource
regulation cycle on Salix lasiolepis because herbivory decreases the
physiological age of S. lasiolepis ramets, resulting in production of
vigorous juvenile shoots preferred by the sawfly, creating a selfperpetuating cycle
galls either stunts or kills shoots. Shoot death or damage
induces the growth of dormant buds from the base of the
plant, which produce juvenile shoots that have rapid vegetative growth and very low production of reproductive
buds in the following growing season. Euura lasiolepis is
univoltine, and the induction of these rapidly growing
young shoots in 1 year results in an increase in the number
of highly preferred oviposition sites where larval survival
is high in subsequent years. In the absence of E. lasiolepis
attack, willow ‘‘branch age’’ would increase. These physiologically older branches produce shorter shoots with
reduced vegetative growth and an increased number of
reproductive buds. The effect of E. lasiolepis attack is to
alter the allocation of willow resources in a way that is
favorable to the sawfly and unfavorable to the willow.
Hjalten and Price (1996) conducted an experimental study
in which artificial pruning of S. lasiolepis induced vigorous
compensatory growth, which led to increased densities of
E. lasiolepis as predicted by the resource regulation
hypothesis.
Euura lasiolepis have a high degree of philopatry. They
usually mate and oviposit in the canopy of the clone from
which they emerge (Price 2003), and experiments have
found that few females disperse more than 8 m (Stein et al.
1994). The distribution of sawflies on a landscape scale
was also consistent with philopatry and limited dispersal
(McGeoch and Price 2005). Thus, there is a strong indication that offspring benefit from changes induced by their
parents on individual willows. Other studies on willows
have documented resource regulation through a juvenilization process whereby herbivore damage induces
Popul Ecol (2010) 52:461–473
dormant bud growth that produces high-quality resources
for herbivores. Euura mucronata is a bud-galler on Salix
cinerea in Finland and has a preference for attacking
young, vigorous shoots and avoids shoots on older
senescing plants (Price et al. 1987a, b). Roininen et al.
(1988) conducted an experiment in which they simulated
herbivory by removing buds on some branches of S. cinerea
and compared them with control branches from which buds
were not removed. They showed that the experimental
branches activated dormant buds that produced rapidly
growing, juvenile shoots and that this resulted in higher
sawfly densities on experimental branches than on controls.
Nozawa and Ohgushi (2002) found evidence of resource
regulation in the spittlebug Aphrophora pectoralis, which
oviposits into stems of several willow species in Japan.
Craig and Ohgushi (2002) found that spittlebugs had a
strong preference for rapidly growing shoots on four willow species and that their performance was higher on these
shoots. Spittlebug oviposition damages or kills the shoot on
which eggs are oviposited, which the following year
stimulates rapid compensatory growth of shoots on the
branch immediately adjacent to the damage (Nozawa and
Ohgushi 2002). These rapidly growing shoots were preferred by A. pectoralis for oviposition, and this leads to
higher egg densities on previously attacked shoots, setting
up a resource regulation positive feedback loop. Early
instar nymphs also prefer to feed on these rapidly growing
shoots immediately adjacent to where they emerge so that
the offspring immediately benefit from the oviposition
damage caused by their mothers (Craig and Ohgushi 2002;
Nozawa and Ohgushi 2002). In addition, there is a strong
correlation between the preference of sites for oviposition,
mating, and feeding (Craig and Ohgushi 2002), indicating a
potentially high degree of philopatry so that several generations could potentially benefit from the resource regulation cycle.
Patterns consistent with the resource regulation
hypothesis have also been found in eucalypts (Landsberg
and Ohmart 1989) to which severe, repeated damage produces juvenile-form foliage that has higher levels of herbivory than adult foliage (Fox and Morrow 1983;
Landsberg and Wylie 1983). Landsberg (1990) found that
the younger foliage on eucalyptus trees suffering from the
dieback syndrome was more nutritious and less well
defended than that on unaffected trees. She suggested that
this increased—quality resource could be the result of a
positive feedback mechanism produced by repeated defoliation that produces juvenile foliage. In another example
from Eucalyptus, Steinbauer et al. (1998) showed that the
coreid bug Amorbus obscuricornis is found at high densities on coppiced Eucalyptus in Tasmania, Australia, and
that shoots on coppiced hosts are of superior quality for
bug performance. The bug destroys apical buds, inducing
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dormant bud activation, and so it may produce a resource
regulation cycle in the absence of coppicing. Other trees
that are coppiced show a similar response, including
coppiced acacia trees in Africa that have much higher
densities of psyllids than normal trees (Webb and Moran
1978). However, these psyllids were only documented as
responding to damage caused by humans, and the research
did not show evidence that they induce dormant bud activation on their own.
Carroll and Quiring (2003) provide another example of
resource regulation, although they do not use that term, in
the interaction of a tortricid moth, Zeiraphera canadensis,
on white spruce, Picea glauca. Moth damage on shoots in 1
year removed apical dominance and activated dormant
buds, which had earlier bud burst than buds on undamaged
shoots. Their data indicated that buds on the damaged
shoots were nutrient sinks and higher quality resources for
larvae that had higher success on damaged buds. More than
40% of buds on damaged shoots were attacked compared
with 10% of buds on undamaged shoots. They suggested
that this was a positive feedback loop as the result of an
evolved strategy by the moth.
Duval and Whitford (2008) found that a cerambycid
beetle, Oncideres rhodosticta, girdles branches of mesquite, Prosopis glandulosa, which induces high levels of
branching through the induction of dormant buds. These
densely branched trees are preferred for further oviposition,
setting up a resource regulation cycle that results in
increasing beetle densities in very densely branched trees
that catch soil and promote dune formation. Dune formation is a key component of desertification so that the
resource regulation process contributes to ecosystem-wide
changes that affect many species.
Resource regulation can interact with induced defenses
to determine resource quality (Kaitaniemi et al. 1997).
Epirrita autumnata is a geometrid moth whose free-feeding
larvae consume apical buds of mountain birch, Betula
pubescens, and the destruction of these buds induces dormant buds that produce larger, higher-quality leaves for
herbivores (Haukioja et al. 1990; Senn and Haukioja 1994).
However, Kaitaniemi et al. (1997) found that the consumption of these leaves did not lead to increased larval
performance in the same summer that growth was induced,
probably because of induced defenses. In the following
year, larval performance did increase slightly, probably due
to amelioration of delayed induced defenses, and so this
process fits the definition of resource regulation.
All of the previous examples of resource regulation are
on woody plants, but in herbaceous plants with multivoltine herbivores there is the possibility for resource
regulation within a single growing season. The lacebug
Corythuca marmorata feeds on goldenrod Solidago
altissima and shows evidence of resource regulation in its
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Fig. 2 The hypothesized linked positive and negative feedback
cycles caused by the lacebug Corythuca marmorata on Solidago
altissima at high densities in its introduced range in Japan. The cycle
is initiated as a positive feedback, resource-regulation cycle. However, when plant resources are depleted, it enters into a negative
feedback phase in which declining resource quality inhibits population growth. The plant may then recover and reenter the positive
feedback cycle. This interaction occurs within a growing season, but
it may provide a model for much longer-term cycles on perennial
plants
introduced range in Japan. The herbivore reaches very high
densities in Japan and has a multivoltine life history.
Goldenrod responds to early herbivore damage by the
induction of branching later in the season (Pilson 1992),
and it also responds by increasing the growth rate of stems
and the production of new leaves (Y. Ando and T.P. Craig,
unpublished data). The lacebug prefers rapidly growing
plants, and so the increased growth initially increased the
growth rate and lacebug attack rate, matching the resource
regulation hypothesis. However, later in the growing
season, continued high lacebug densities led to a decrease
in plant growth and a decreased preference for plants that
had suffered high levels of previous attack. This indicates
that high densities may induce a negative feedback loop
and the interaction may fluctuate between positive and
negative feedback loops (Fig. 2).
In contrast, the only other study testing the resource
regulation hypothesis on an annual plant by Dhileepan
(2004) found no evidence of resource regulation in the
stem-galling moth Epiblema stenuana, a moth that has
multiple generations on annual herbaceous aster Parthenium hysterophus. The moth attacked the most vigorous
plants, but the presence of galls did not increase growth or
attack by subsequent generations of the galler.
Mammals and resource regulation
Mammalian herbivores are involved in positive feedback
loops with plants in a range of interactions (Bergqvist et al.
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2003). Mammalian browsers induce compensatory growth
by browsing plants and inducing growth of dormant meristems, which can produce a positive feedback loop that
maintains or increases the availability of high-quality
resources. This process is very similar to the resource
regulation process in insects, although that term had not
been applied to these interactions. McNaughton’s (1976,
1979) pioneering studies showed that grazing by migrating
herbivores in the Serengeti maintain a lawn of high-quality
resources. Wildebeest grazing of grasses prevents senescence and increases primary production and plant quality
that benefits subsequent grazers, including gazelles
(McNaughton 1976). Grazing may occur at a rate that
optimizes the production of palatable grasses for the herbivores (McNaughton 1979). However, whereas the same
species benefit from the improved grazing, there is no
indication that the same individuals or their relatives graze
the same plants.
Moose, Alces alces, prefer to browse on compensatory
growth produced in response to previous browsing, and
the same or related individuals may benefit from this
rebrowsing. Danell et al. (1985) found that when moose
browsed on birches, Betula pendula and B. pubescens,
they induced dormant buds to produced shoots that were
higher in nutrition and longer than unbrowsed shoots.
Browsing also maintained shoots at a height at which they
were more accessible for grazing in subsequent years than
foliage on unbrowsed plants. Bergqvist et al. (2003) found
that previously moose-damaged Scots pines, Pinus sylvestris, were 3.5 times more likely to be browsed than
undamaged trees, although the relative preference dropped
as the proportion of all trees browsed increased. There are
good indications that the same individuals or offspring of
the individuals benefit from this resource regulation.
Moose utilize the same summer home ranges repeatedly,
and their calves usually accompanied females to their
home range and then resided close to them as adults
(Cederlund et al. 1987). Home ranges of offspring widely
overlapped with their natal home range for several years
(Cederlund and Sand 1992), so offspring probably browse
on compensatory growth induced by their mothers. Moose
also returned to the same winter ranges (Sweanor and
Sandgren 1989).
Snowshoe hares browsing on felt leaf willow, Salix sp.,
which induces dormant bud growth, has a complex effect
on future resource quality. Winter hare browsing increased
the nutrient quality of willows in the following summer
(Bryant 2003), but it decreased willow quality 2–3 years
following herbivory (Fox and Bryant 1984; Bryant et al.
1985). This provides evidence of a complex cycle in which
an initially positive feedback cycle changes into a negative
feedback cycle similar to that proposed for some insects
(Fig. 2).
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species. In a similar example, African elephants,
Loxodonta africana, prefer to browse previously damage
trees, and there was a strong preference for trees that had
been artificially clipped 3 years prior to a choice experiment (Makhabu and Skarpe 2006).
Generality of resource regulation
Fig. 3 Positive feedback cycle caused by severe browsing by large
mammals on woody plants (redrawn from Du toit et al. 1990). The
arrows between levels indicate positive effects except for those
marked with a negative sign (-). The :; arrows indicate the direction
of change within each level
Other mammals may also induce resource regulation
cycles that benefit their offspring. Du Toit et al. (1990)
found that severe browsing by impala, Aecpyceros melampus, and giraffes, Giraffa camelopardalis, on Acacia
nigrescens reduced the physiological age of plant modules
in the acacia, increased food quality, and perpetuated further feeding, creating a positive feedback loop (Fig. 3) that
is very similar to that found in insects (Fig. 1). The palatability of the Acacia foliage increased because of the
twigs and branches that regrew after herbivory had higher
nutrient levels. The high carbon demands of regrowth
reduced the production of secondary metabolites, resulting
in reduced condensed tannin content. Fornara and Du Toit
(2007) found that continuous heavy grazing selected for
trees that had higher levels of tolerance, resulting in a
strong regrowth potential in trees in heavily browsed areas
compared with trees in low herbivory areas. The same trees
tended to be heavily grazed repeatedly when they were
near waterholes, and the authors argued that continuous
browsing pressure has probably been maintained in these
areas for hundreds of years. Thus, acacia trees could be
maintained in a more palatable condition for long periods,
benefiting generations of herbivores (Fornara and Du Toit
2007). Whether this would benefit descendents of earlier
grazers depends on the degree of philopatry in these
Juvenilization through dormant-bud activation, resulting in
resource regulation, is likely to be a common interaction,
although this hypothesis has only been tested in relatively
few systems. It may have repeatedly evolved because it
allows herbivores to exploit a common plant reaction in
response to a wide range of damage and disturbance. It
would be difficult for plants to evolve to alter this general
response due to selection by an herbivore, as it provides the
plasticity for plants to respond to many kinds of damage.
The carbon/nutrient balance hypothesis predicts that plants
in high-resource, highly competitive environments will
evolve a fast-growing plant syndrome in which plants
respond to damage with vigorous regrowth and inducible
defenses (Coley et al. 1985). Many plants involved in the
resource-regulation-through-juvenilization cycle fit the
fast-growing plant syndrome. However, in many of these
interactions, there is no evidence of induced defenses;
instead, herbivores have better performance on vigorously
growing compensatory growth (Price 2003). Three
assumptions necessary for resource regulation to occur are
frequently met, indicating it may be a widespread phenomena: (1) Many plants respond to damage with dormant
bud activation that produces vigorous juvenile growth. (2)
Herbivores have a strong preference for, and high performance on, rapidly growing juvenile plant modules. (3) The
same individual plants are repeatedly attacked by an herbivore species.
The first assumption is frequently met, as many plants
maintain a pool of dormant buds activated when plants are
damaged and produce juvenile growth (Haukioja et al.
1990). Juvenile tissue is produced in response to herbivory
as a result of the basic organization of plants as modular
organisms that have a hierarchy of meristems, which
determines resource allocation. When dominant meristems
are removed by herbivory or other causes, subordinate
meristems can be activated that produce compensatory
growth (Watson and Casper 1984; Benner 1988; Thomas
and Watson 1988). Haukioja et al. (1990), Tuomi et al.
(1994), and Nilsson et al. (1996) all developed models
indicating that the maintenance of dormant buds is a bethedging strategy that allows plants to respond to periodic
high levels of herbivore damage. For resource regulation to
occur, dormant bud growth induced by herbivory must
produce growth with juvenile characteristics. The modular
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nature of plants means that in contrast to animals, plants
can be a mosaic of repeated module tissues with different
age-related characteristics (Kearsley and Whitham 1989,
1998). The horticultural literature shows that there are two
types of age-related character changes in plants: ontogenetic and developmental (reviewed in Kearsley and
Whitham 1989, 1998). Ontogenetic or maturational changes result from modification of gene activity in meristems
that alters the characteristics of the organs they produce,
whereas the developmental changes resulting in physiological aging are processes that result from senescence,
which is produced by the inability of a plant to support all
of its parts for a variety of reasons ranging from imbalances
among tissues or the complexity of vascular tissues
(Fortanier and Jonkers 1976). Physiologically juvenile tissues typically have a suite of characteristics, including a
lack of reproductive buds, ease of adventitious rooting, and
high vigor. The loss of juvenile characteristics, particularly
vigor, is associated with the increased complexity of the
vascular system and the increased distance between shoots
and meristems and roots (Borchert 1976). Physiological
aging effects can be reversed by pruning or propagation,
but ontogenetical aging is not altered when cuttings are
asexually propagated (Wareing 1959; Borchert 1976;
Fortanier and Jonkers 1976). The specific tissues utilized
by herbivores will determine whether a resource regulation
cycle will be initiated. Herbivores that damage ontogenetically mature growth will not induce vigorous regrowth,
as this damage will activate mature meristems that will
produce mature regrowth. For example, the aphid Pemphigus betae has a strong preference for ontogenetically
mature regions of cottonwood trees (Kearsley and Whitham 1989, 1998), and any regrowth they activated would
be of mature leaves. Plants that maintain a population of
dormant buds in physiologically juvenile zones of the plant
will be susceptible to the induction of a resource-regulation
cycle, and this is likely in plants adapted to high-disturbance environments. Resource regulation will occur when
herbivore damage induces resprouting near the base of the
plant where there is a short distance between the meristem
and the roots and a low complexity of vascular system
connections. The modular nature of plants means that
compensatory growth and particularly the induction of
dormant buds depend on damage to the integrated physiological unit (IPU), so that the response will be highly
localized (Watson 1986). Because vigorously growing
modules are likely to be found in physiologically immature
zones of the plant, an herbivore preference for these
modules is likely to produce local damage that results in
the production of juvenile growth. As compensatory juvenile growth is a generalized response to damage by abiotic
factors such fires and flood, as well as herbivory, this is an
important factor in the initiation of a resource regulation
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cycle. Salix lasiolepis maintains a large population of
dormant buds in physiologically juvenile tissue, and
these are more frequently activated by flood damage than
E. lasiolepis damage, but the sawfly may colonize these
flood-damaged shoots and initiate a resource-regulation
cycle (Craig et al. 1988).
The second assumption of the juvenilization hypothesis,
that herbivores have high densities on vigorously growing
plant modules, has been extensively supported (Price
1991). In his most recent review Price (2003) has shown
extensive support for this hypothesis, with 122 insects
showing a positive response to plant vigor: 38 sawflies that
respond positively to shoot length, 28 other gallers with a
positive response to plant vigor, and 56 other arthropods
that have been demonstrated to have higher densities on
vigorous plant modules, young plants, or plants with high
metabolic activity. As Price (2003) points out, this is an
unusually comprehensive test of a hypothesis in a wide
variety of interactions. There is strong support for this
pattern in endophagous insects such as gallers, borers, and
miners, but the list also includes leaf-rollers, flower-head
dwellers and free feeders such as cercopids, mites, and
aphids. The preference for vigorous plant modules thus
appears to be a widespread pattern.
The third assumption, that the same individual plants
will be repeatedly attacked by the same herbivore species,
is more difficult to test, as there are few long-term studies
of the population dynamics of insects on individual plants.
Price (2003) found strong correlations of E. lasiolepis
densities on Salix lasiolepis clones among years. Ohgushi
and Sawada (1985) found evidence of very low dispersal
rates and long-term population stability of an herbivorous
lady beetle, Henosepilachnia niponica, indicating consistent reuse of its perennial thistle Cirsium kagamontanum
host plants. Highly sessile insects such as scales also
consistently utilize the same host plants and may even form
demes adapted to individual plants (see references in
Mopper and Strauss 1998).
Maintenance and termination of resource regulation
cycles
Positive feedback cycles result in increasing herbivore
density, and increasing plant damage will eventually lead
to the exhaustion of plant resources and termination of the
positive feedback cycle. There is no mutualism between
plants and herbivores: the juvenilization cycle is costly to
the plant, even when it produces vigorous vegetative
growth, because it can decrease plant fitness by decreasing
sexual reproduction and vegetative spread (Sacchi et al.
1988). Plants can increase vegetative growth under some
conditions until an excessive level of defoliation inhibits
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growth (reviewed in McNaughton 1979). If some biotic or
abiotic factor other than host plant quality maintains herbivory below the threshold level above which plants cannot
regrow lost tissue, then a resource regulation cycle could
be maintained indefinitely. A resource regulation cycle
could be maintained for a limited time, even when a plant’s
tolerance limit was regularly exceeded, if the plant had
reserves to draw on.
Plant–herbivore interactions may alternate between
positive and negative feedback cycles. Herbivore density
may increase in a positive feedback cycle until damage
exceeds the limits of the plant to compensate for tissue
loss, and then a negative feedback loop may be initiated.
Herbivore density would then decline continually until the
population dropped below the plant’s tolerance limit,
allowing the plant to recover and a positive feedback to
resume. Plant regrowth and herbivore populations may be
in a dynamic equilibrium, resulting in cyclic interaction of
insect population density and plant module quality (Fig. 2).
Plants may be caught in a juvenilization cycle because
herbivores can take advantage of a general strategy that
plants have evolved for compensating for any kind of
damage. Plants can respond to herbivory with either
defense or tolerance. Tolerance has been defined as a
strategy that plants have evolved to minimize loss of fitness
by regrowing and/or reproducing after herbivory (Strauss
and Agrawal 1999), and it may include flexible rates of
nutrient absorption, photosynthesis, and growth as well as
numerous protected meristems (Sharpe and Hester 2008).
What is termed tolerance to herbivory may actually be a
very general compensatory response to any kind of damage, including flood, wind, trampling, disease, and fire
(Belsky et al. 1993; Rosenthal and Kotanen 1994).
Resource-regulating herbivores can exploit this general
response to their advantage, and an unresolved question is
why plants do not evolve a specific defense against these
herbivores. Coley et al. (1985) predicted that plants with a
rapid growth strategy would protect their compensatory
growth with induced defenses, but plants frequently do not
do so. I suggest two reasons why defenses have not evolved
in response to resource regulation: first, the benefits of
investment in defense may be lower than investment in
compensatory growth; second, plants may lack the ability
to distinguish herbivory from other sources of damage,
making investment in defense frequently maladaptive.
Tolerance may be a better strategy than defense if
resource regulation cycles are rare and short-lived, providing a low return on investment in defense. This could
occur if resource regulation cycles are frequently terminated by non-plant-related factors limiting the return in
investment in defense. Plants could escape from a resource
regulation cycle due to abiotic conditions, including
drought, fire, or flood, that lead to a decline in herbivore
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populations and negate the need to invest in defense. The
population density of E. lasiolepis is strongly limited by
abiotic factors, and as a result, only a small proportion of
plants have high population densities in any 1 year (Craig
et al. 1988; McGeoch and Price 2005; Price and Hunter
2005). Population density is strongly correlated with the
water available to the plant: even those populations on
plants with high population densities where resource regulation occurred suffered large declines during extreme
droughts (Price and Hunter 2005). A resource regulation
cycle could also be ended or diminished in its strength by
biotic factors such as an increase in mortality due to natural
enemies.
Activation of dormant buds that produce rapidly growing, undefended shoots may be adaptive in resource-rich
environments, such as riparian areas, where there is intense
competition with other plants for light and space (Rosenthal
and Kotanen 1994). For example, Craig et al. (1988)
showed that for the arroyo willow, extensive damage caused
by flooding is much more frequent than damage by sawfly.
Willows face intense competition to rapidly regrow in order
to compete for space and light following flooding, and so
investment in growth would always yield large benefits.
Undefended growth only rarely leads to increased sawfly
attack, because E. lasiolepis has a highly patchy distribution
(Craig et al. 1988) combined with poor dispersal (Stein et al.
1994) that results in susceptible rapidly growing shoots
frequently escaping being galled (McGeoch and Price
2005). Thus, relatively rare and patchily distributed herbivores may be able to take advantage of the generally
adaptive response of undefended dormant bud growth to
induce a resource regulation cycle without inducing a
defensive response.
Similarly, grasses in the tall-grass prairies of North
American have evolved protected meristems that rapidly
regrow and produce palatable food for bison following fire
or for bison herbivory (Dalgleish and Hartnett 2009). In
presettlement times, fire was frequent and covered very
large areas, whereas bison grazing was highly patchy in
space and time (Knapp et al. 1999). As a result, investment
in defense, which would not protect against fire and which
would only rarely defend against bison regrazing, may not
have been favored, and instead, the plants invested in tolerance that would be adaptive in response to both causes of
damage.
Induced defenses are not effective unless plants can
distinguish damage from a specific herbivore that would be
susceptible to the defense from all other damage. If damage
by a specific herbivore is costly, widespread, and predictable, such as is the case for felt-leaf willows eaten by arctic
hares (Bryant 1981), then induced defenses will evolve.
However, investing in an induced defense for a compensatory growth response to damage from an herbivore that is
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468
not susceptible to that defense or an abiotic factor would be
maladaptive. Relatively rare and patchily distributed herbivores are unlikely to lead to the evolution of induced
defenses, even if damage is high on individual plants.
Resource regulation may evolve because of asymmetry
in the interaction between some herbivores and plants
(Craig et al. 1988). Resource regulation may be important
in the evolution of herbivore strategies and in determining
their population dynamics. In contrast, the impact of
resource regulation on the evolution of plant strategies and
population dynamics may be relatively low.
Resource regulation by nutritional or chemical
alteration
Alteration of the nutritional quality or defenses of plants
without the induction of dormant buds may also result in
resource regulation. A solitary bark beetle Dendroctonus
micans repeatedly attacked the same spruce trees in different years, and Gilbert et al. (2001) suggested that a
reduction in defensive pitch production capabilities was
responsible for the beetle’s oviposition preference for
previously attacked trees. Several studies have suggested
that improved nutrition in regrown leaves results in repeated attacks on the same plants. Rockwood (1974) found
that when a tropical tree was hand-defoliated, the regrowth
leaves suffered up to 100% herbivory by a flea beetle, and
in response to this beetle, defoliation a second regrowth of
leaves was again heavily attacked by the beetle. Rockwood
suggested that the nutritional and chemical defenses in
regrowth leaves had been altered. Williams and Myers
(1984) and Roland and Myers (1987) found that larvae on
trees that had been moderately defoliated in 1 year had
better performance the following year on those trees.
Williams and Myers (1984) proposed that increased
nutritional quality of the plant increased performance and
suggested that the improvement could be due to an increase
in soluble nitrogen in response to host-plant stress, as
proposed by White (1974, 1978). Roland and Myers (1987)
suggested that in addition to improved nutrition, alteration
of bud phenology and increased compensatory growth rates
led to increased larval performance. Wallner and Walton
(1979) showed that pupal weights of gypsy moths,
Lymantria dispar, on black oak, Quercus velutina, were in
some cases higher on twice-defoliated oaks than on oncedefoliated oaks but lower than oaks that had not been
defoliated at all. Several other studies have shown that
artificial defoliation leads to increased preference or performance on plant regrowth (Pullin 1987; Wilcox and
Crawley 1988; Potter and Redmond 1989; Messina et al.
1993) due to a change in foliage nutrition or chemical
defenses. Feeding by mites, Tetranychus urticae, has been
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Popul Ecol (2010) 52:461–473
shown to increase subsequent feeding (English-Loeb and
Karban 1991), but Karban and Niiho (1995) found that
feeding on apical leaves and not cotyledons increased
subsequent herbivory, and these patterns could be the result
of an alteration of the plant’s chemical or nutritional
characteristics.
Resource regulation by resource manipulation
Resource manipulation can alter the distribution of
resources, leading to improved growth or nutritional
quality in ways that increase the probability of further
attack and which could result in resource regulation.
Gallmakers can be sinks for resources in plants (Weis and
Kapelinski 1984; Tscharntke 1989; Larson and Whitham
1991, 1997; Fay et al. 1996), thus altering plant growth and
potentially the distribution of subsequent attack. Craig
et al. (1990) showed that a gall forming in one internode
increased shoot growth in distal internodes on a shoot and
increased the probability of oviposition on those nodes.
They termed this resource facilitation, and the effects have
only been documented in interactions within a generation.
However, if the effect of resource sinks persist from
one year to the next, they can potentially produce a
resource regulation cycle. Price and Louw (1996) documented how a gall-forming weevil, Urodontus scholtizi,
altered the growth of its host plant Galenia africana by
diverting resources to galled stems. These stems grew more
vigorously after being galled, and adjacent ungalled stems
frequently died. Although the oviposition preference of
subsequent generations was not measured, they suggest
that a preference for vigorous growth could result in
resource regulation.
Prado and Vieira (1999) found that the stem-galling
midge, Neolasioptera sp., that induces galls on a small tree
Eremanthus erythroppapus in Brazil, produced more galls
on longer, thicker branches and that these branches had
more galls in subsequent years. The aggregation of currentand previous-year galls on vigorously growing shoots is
consistent with the resource regulation hypothesis, with
galls increasing the rate of shoot growth and increasing
subsequent galling. However, very high densities of galls
led to a decrease in galls in subsequent years.
The long-term impact of herbivores in the alteration of
plant architecture and resource distribution by resource
manipulation needs much more study to determine whether
it can result in resource regulation. It is likely that in many
cases, resource regulation by resource manipulation is
unrecognized, as there have been few studies that have
taken the multigenerational measurements necessary to
detect its existence. The potential for resource regulation
by resource manipulation is high, as some herbivores
Popul Ecol (2010) 52:461–473
always manipulate their host plants to some degree. For
example, all gallers divert resources from normal plant
functions to gall formation.
Population dynamics
Resource regulation has the potential for influencing the
population dynamics of herbivores by stabilizing and
maintaining populations at high densities. In the case of
juvenilization, in the absence of the positive feedback
cycle, individual plants would rapidly grow out of the
vulnerable juvenile stage (Fig. 1), leading to decline and
even local extinction of insect populations. The stability of
Euura lasiolepis populations is partially the result of
resource regulation, and it appears capable of maintaining
stable densities indefinitely (Price 2003). Resource regulation interacts with abiotic factors to maintain stable
population densities: the population densities are strongly
correlated with high winter precipitation, which promotes
rapid shoot growth (Hunter and Price 1998). Individual
willows in sites with abundant water maintain stable high
densities partly as the result of resource regulation. However, it seems likely that if a sawfly population colonized a
plant that was in a juvenile condition due to disturbance,
the positive feedback mechanism would increase the population density. In insect species in which there is a strong
preference for juvenile tissue in the absence of resource
regulation, high-population herbivore densities are transient unless rejuvenation occurs by disturbance, such as fire
(Washburn and Cornell 1981) or coppicing (Landsberg
1988).
A second effect of positive feedback cycles, such as
resource regulation, is to increase resource heterogeneity
(Hunter 1992; Hunter and Price 1992). In the absence of
positive herbivore feedback cycles that keep some plant
modules in a juvenile state, the composition of plant
resources would become more uniform. In the case of the
S. lasiolepis–E. lasiolepis interaction, the willow would
achieve an older, more uniform, distribution in the physiological age of shoots. In other systems, the loss of apical
dominance and the induction of dormant lateral buds
change the plant physiological age structure and plant
architecture that create greater resource diversity.
Evolution and coevolution of resource regulation
interactions
Is resource regulation a strategy evolved by herbivores to
induce plant susceptibility for their offspring, or is it
merely an incidental effect of plant damage that is an
inevitable effect of herbivory? The most parsimonious
469
explanation of the evolution of resource regulation is that it
results from an herbivore strategy that has evolved to
increase fitness directly by selecting plant tissue that can be
eaten where their own or their offspring’s performance is
high. The damage caused by this feeding coincidently
induces a generalized plant response that is adaptive for the
plant under most circumstances but that in some cases
benefits some herbivores by producing more tissue preferred by that herbivore. Hypothetically, if there is a high
degree of philopatry, then herbivores could be selected to
induce changes in plant growth that increase their inclusive
fitness by increasing the fitness of grand-offspring and
other more distantly related individuals that use the same
plant. However, unless dispersal is very low, these inclusive fitness gains are likely to be much smaller than direct
fitness gains.
Generating unique predictions that would differentiate
between the hypotheses that herbivore strategies evolve
due to selection for increases only in direct fitness, or
whether there is selection for both direct and inclusive
fitness, is difficult. An examination of the E. lasiolepis–S.
lasiolepis interaction illustrates these difficulties. In
E. lasiolepis, oviposition preferences and gall characteristics have been shown to increase offspring fitness (Craig
et al. 1986, 1989, 1990). Do these oviposition preferences
and gall characteristics also evolve because they increase
the fitness of subsequent generations because they induce
dormant bud growth in subsequent years? Large, rapidly
growing galls provide protection against parasitoids (Price
and Clancy 1986; Craig et al. 1990; Craig 1994), but large
galls could also increase shoot damage and increase the
induction of dormant buds. Females preferentially oviposit
on the longest shoots because this increases their offspring’s chances of survival (Craig et al. 1989), but damaging long shoots may also be more likely to induce
dormant bud growth than if sawflies preferred and damaged
short shoots. Oviposition in a node immediately distal to a
previously galled shoot increases survival of offspring in
that gall (Craig et al. 1990), but multiple galls are more
likely to kill shoots and induce dormant buds (Craig et al.
1986). The stimulation of dormant bud growth would have
no effect on the fitness of the offspring of a female, but it
has potential to increase fitness of their grand-offspring,
which has not been measured.
Similar questions could be asked about mammalian
grazers. Do they feed in a manner that only maximizes
their immediate acquisition of food, or do they graze in a
manner that increases production of food in the following
year? In resource manipulators, the question is whether
the diversion of resources to the area of the plant with a
gall only benefits the first generation or whether subsequent generations also benefit from changes in plant
growth.
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470
One experimental test of the hypothesis that the feeding
strategy of herbivores has evolved to benefit subsequent
generations would be to compare the fitness of herbivores
in treatments with and without the effects of resource
regulation on the second generation. In one treatment,
herbivores would be reared on the same plants for two
generations so that offspring would utilize plants in which
resources had been altered by the first generation. In the
second treatment, the herbivores would be moved to plants
that had been protected from damage during the first generation. If the total fitness of a female’s grand-offspring in
the first treatment were higher than total fitness in the
second, it would support the hypothesis of selection for
resource regulation behaviors. A second requirement for
the evolution of resource regulation as an evolved strategy
is that offspring benefit from the resource susceptibility
induced by their parents. The intergenerational relatedness
of individuals involved in resource regulation has never
been measured, and development of methods for measuring
the relatedness of individuals using the same plant in
subsequent generations would enable testing of this
hypothesis.
Resource regulation and interspecific interactions
Alteration of architecture, physiological age, chemistry,
and nutrition of plants involved in resource regulation
could potentially have a wide-ranging impact on other
species. Whereas it has not been directly linked to resource
regulation, browsing and induced dormant bud production
has led to increased herbivory by other species. Moosebrowsed plants have higher densities of psyllids, leaf gallers, leaf miners, and aphids than unbrowsed plants (Danell
et al. 1985). Roininen et al. (1997) found that browsing by
snowshoe hares and moose led to an increase in gallers on
arctic shrubs. Olofsson and Strengbom (2000) found that
reindeer browsing on willows increased the density of gallforming mites and insects. Utsumi and Ohgushi (2007,
2008) documented the effect of ghost moths that induced
adventitious growth, which benefited beetles. Eventually,
the positive feedback loops involved in resource regulation
and induced susceptibility need to be incorporated in our
understanding of population dynamics and community
structure.
The widespread existence of such indirect plant-mediated interactions among species has only recently been
recognized, but there is growing evidence that they are
potentially very important in structuring interspecies
interactions and communities (Ohgushi 2005; Ohgushi
et al. 2007). Duval and Whitford’s (2008) demonstration
that a resource regulation interaction could produce
desertification is an indication of the potential for
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Popul Ecol (2010) 52:461–473
community-wide impacts of such interactions. The intricate
and connected negative and positive feedback loops both
within and among species mediated by host-plant effects
are complex and difficult to measure, but they are
increasingly recognized as being important (Ohgushi
2005). Understanding these feedback loops is important
because indirect interactions that determine population
densities may be crucial in determining the structure of
ecological communities (Ohgushi et al. 2007).
Conclusions
Resource regulation has been demonstrated in a variety of
plant–herbivore interactions, and it is one of a wide range
of positive feedback cycles whereby herbivory increases
plant resource quality for subsequent herbivores. A range
of mechanisms may produce this positive feedback cycle,
including induction of dormant meristems, resource
manipulation that alters source-sink relationships within
plants, and alteration of plant nutritional quality or defenses by herbivory. Herbivores involved in resource regulation include insects and vertebrates and include
endophages, browsers, and grazers. These positive feedback cycles may be linked to negative feedback cycles,
producing complex temporal fluctuations in herbivore
densities and plant quality.
Whereas the work to date indicates the potential
importance of resource regulation and other positive
feedback cycles in plant–insect interactions, further
research is needed to increase the understanding of their
ecological and evolutionary implications. The population
dynamics and spatial distribution of herbivorous insects is
largely determined by the sum of their interactions with
individual plants through time. However, long-term records
of insect densities on individual plants necessary to
understand positive and negative feedback cycles are rare.
One exception is research on Euura lasiolepis summarized
by Price (2003), on which we relied in this review. Price
asserts that the mechanisms determining the population
dynamics of this species are better understood than in any
other species. Similar studies on a range of interactions that
carefully follow the relationship between the variation in
individual plant resources and herbivore fitness through
time are needed. Research on herbivore philopatry is
lacking and is needed to understand the evolutionary and
coevolutionary implications of positive feedback loops.
Such detailed accounting of individual plant module
quality and herbivore fitness and dispersal has not been
traditionally included in studies of herbivore population
dynamics, but a focus on these details may uncover the
mechanisms that explain broad patterns in population
dynamics and the coevolution of plant–insect interactions.
Popul Ecol (2010) 52:461–473
Acknowledgments I thank Sunshine Carter, University of Minnesota
Duluth Librarian, for assistance in searching the literature. Joanne K.
Itami, Peter W. Price, Osamu Kishida, and two anonymous reviewers
provided helpful advice and comments on drafts of the manuscript.
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