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INTEG. AND COMP.BIOL., 42:892–908 (2002)
Environmental Stress, Bottom-up Effects, and Community Dynamics:
1
Integrating Molecular-Physiological and Ecological Approaches
2,
BRUCE A. MENGE, *ANNETTE M. OLSON,* AND ELIZABETH P. DAHLHOFF†
*Department of Zoology, Oregon State University, Corvallis, Oregon 97331-2914 and
†Department of Biology and Center for Environmental Studies, Santa Clara University, Santa Clara, California 95053
SYNOPSIS. Environmental stress and nutrient/productivity models predict the responses of community
structure along gradients of physical conditions and bottom-up effects. Although both models have succeeded
in helping to understand variation in ecological communities, most tests have been qualitative. Until recently,
two roadblocks to more quantitative tests in marine environments have been a lack of (1) inexpensive, field-
deployable technology for quantifying (e.g.) temperature, light, salinity, chlorophyll, and productivity, and Downloaded from https://academic.oup.com/icb/article/42/4/892/659154 by guest on 18 August 2022
(2) methods of quantifying the sub-organismal mechanisms linking environmental conditions to their eco-
logical expression. The advent of inexpensive remote-sensing technology, adoption of molecular techniques
such as quantification of heat-shock proteins and RNA:DNA ratios, and the formation of interdisciplinary
alliances between ecologists and physiologists has begun to overcome these roadblocks. An integrated eco-
physiological approach focuses on the determinants of: distributional limits among microhabitat patches
and along (local-scale) environmental gradients (e.g., zonation); among-site (mesoscale) differences in com-
munity pattern; and geographic (macroscale) differences in ecosystem structure. These approaches promise
newinsights into the physiological mechanisms underlying variation in processes such as species interactions,
physical disturbance, survival and growth. Here, we review two classes of models for community dynamics,
andpresent examples of ecological studies of these models in consumer-prey systems. We illustrate the power
of new molecular tools to characterize the sub-organismal responses of some of the same consumers and
prey to thermal stress and food concentration. Ecological and physiological evidence tends to be consistent
with model predictions, supporting our argument that we are poised to make major advances in the mech-
anistic understanding of community dynamics along key environmental gradients.
INTRODUCTION dients, and that those in the most austere environments
What are the determinants of community structure? (i.e., those having the harshest physical conditions or
This is a central question in ecology, and despite great the lowest productivity), will have simple communities
progress, a synthetic model of the causes of patterns whose structure is determined directly by severe stress
of distribution, abundance, diversity, size structure, or nutrient shortage. Increasing moderation in environ-
and spatial pattern remains elusive. Two classes of mental conditions leads to increased abundances, more
conceptual models that provide a context-dependent complex trophic structure, and increased influence of
framework for understanding, and hopefully predicting species interactions on structure (Menge, 2000; Menge
community dynamics have been termed ‘‘environmen- and Branch, 2001).
tal stress models’’ and either ‘‘nutrient/productivity These models are venerable, having been proposed
models’’ or the ‘‘food chain dynamics hypothesis’’ in the late 1970s, and their roots go back even further,
(Connell, 1975; Menge and Sutherland, 1976, 1987; to the well known model of Hairston et al. (Hairston
Fretwell, 1977, 1987; Grime, 1977; Oksanen et al., et al., 1960). Both types of model have succeeded in
1981; Menge and Olson, 1990; Menge, 2000; Menge helping to understand variation in community struc-
and Branch, 2001). Environmental stress models as- ture, but most tests to date have been qualitative. Why
sume that community structure results from species in- haven’t we progressed more rapidly in developing a
teractions and disturbances, and how these are modi- more quantitatively based literature on context-depen-
fied by underlying gradients of environmental stress dent community dynamics? We suggest that until re-
(where stress is a consequence of environmental con- cently, progress was hindered by three major road-
ditions such as temperature, moisture, salinity, etc.). blocks. First, we have lacked reliable, inexpensive, and
Similarly, nutrient/productivity models also assume field-deployable equipment for quantifying environ-
that community structure results from species inter- mental conditions. Second, methods of quantifying the
actions, but emphasize the role of bottom-up factors sub-organismal physiological processes, or mecha-
(nutrients, productivity) as determinants of variation in nisms, that underlie the ecological responses to stress
the effects of interactions. Both models postulate that or nutritional conditions under field conditions were
communities can be ordered along environmental gra- generally unavailable. Third, there was little encour-
agement to form the alliances among individuals in the
1 From the Symposium Physiological Ecology of Rocky Intertidal relevant biological subdisciplines that would permit
Organisms: From Molecules to Ecosystems presented at the Annual the application of appropriate expertise to what was
Meeting of the Society for Comparative and Integrative Biology, 2– fundamentally an interdisciplinary problem.
7 January 2002, at Anaheim, California.
2 E-mail: mengeb@bcc.orst.edu During the past decade, important progress has been
892
INTEGRATING ECOLOGY AND PHYSIOLOGY 893
madeinremovingthesehindrancestoprogressinecol-
ogy. The advent of the microchip underpinned dra-
matic strides in affordable, conveniently-sized and
sturdy remote-sensing technology, including devices
that can record continuously, at appropriate temporal
scales, temperature, light, salinity, chlorophyll-a, and
productivity (or their proxies). Simultaneously, the rise
of molecular biology has led to the development of
potentially powerful techniques to quantify organismal
response to stresses or to the food environment (Cole-
man et al., 1995; Somero, 1995; Feder and Hofmann,
1999). In particular, these measures (e.g., heat shock
proteins, RNA:DNA ratios) offer insight into sublethal
and/or subtle and/or short-term responses that can be Downloaded from https://academic.oup.com/icb/article/42/4/892/659154 by guest on 18 August 2022
impossible or at least difficult to quantify, especially
on short time scales, using standard ecological mea-
sures (e.g., growth, survival, reproduction). Finally,
growing awareness of the potential power of a hybrid,
interdisciplinary approach to mechanistic studies of
community dynamics has led to increased cross-fertil-
ization among relevant subdisciplines in collaborative
studies of eco-physiology in an experimental field con-
text. FIG. 1. Environmental stress models (simplified, after Menge and
Here we examine these issues, with the dual goals Olson, 1990). In consumer stress models (CSMs), consumers are
of evaluating the current state of the art, and suggest- assumed to be more affected by stress than are prey. In prey stress
ing possible future directions for research. We first re- models (PSMs), consumers are assumed to be less affected by stress
view two classes of environmental stress models and, than are prey. As stress moderates, basal species control by consum-
ers occurs either under the most benign conditions (CSM) or inter-
to test the predictions of these models, we present field mediate stress conditions (PSM). Effective food chain length
experiments that illustrate the effects of stress on con- (EFCL)refers to whether no species are present (EFCL 5 0), species
sumer-prey interactions. We then consider recent stud- are present but scarce (EFCL 5,1), one trophic level (basal species
ies that have aimed at examining externally undetect- or consumer) is dominant (EFCL 5 1), or both levels are abundant
able, sub-organismal responses to stress or nutritional (EFCL 5 2).
conditions, and linking them to the ecological field ing stress, EFCL increases, with first one, then two
context in which the responses occur. effective levels.
MODELS OF COMMUNITY STRUCTURE As proposed by Menge and Olson (1990), the pre-
Environmental stress models dictions of the ESM depend on whether the consumer
We first consider a simple two-level food chain, or the prey is most strongly affected. Consumer Stress
with consumers (e.g., herbivores or primary carni- Models (CSMs) describe changes in trophic structure
vores) and prey (e.g., plants or basal species) (Fig. 1). and relative impacts of interactions under the assump-
The term ‘‘basal species’’ (Pimm, 1982) accommo- tion that consumers are more severely affected by
dates sessile marine invertebrates into this scheme. stress than are their prey (Fig. 1, left panels). Such a
Trophically, sessile marine invertebrates are herbi- difference can arise when consumers are larger than
vores/detritivores, but as space users, they are ecolog- their prey, are unable to shelter when conditions be-
ically more comparable to benthic macroalgae, and come harsh, or too slow-moving to temporarily vacate
like macroalgae, obtain resources from the water col- the habitat for locations with more moderate condi-
umn. Thus, for example, in marine communities, both tions (Menge, 1978a, b; Denny et al., 1985; Menge
limpet-alga and whelk-barnacle interactions are two- and Sutherland, 1987; Denny, 1988). With stress, con-
level food chains. sumers devote the majority of their resources to stress
responses and are therefore ineffective in controlling
Wenext consider how food chain length (equivalent prey, making EFCL 5 1 (Fig. 1 left, top and middle
to trophic complexity) varies along monotonic envi- panels).
ronmental gradients of ‘‘environmental stress’’ (or be- Prey Stress Models (PSMs) describe changes ex-
low, ‘‘productivity’’). In the Environmental Stress pected under the assumption that prey are more se-
Model (ESM), under the most stressful conditions, no verely affected by stress than are their consumers (Fig.
organisms can persist (Fig. 1). With moderation, or- 1, right panels). Such a difference can arise when con-
ganisms can colonize, but are still too scarce for in- sumers are smaller than their prey, can find shelter near
teractions to have an impact (effective food chain prey (or on/under the prey itself), or are fast-moving
length 5 EFCL ,1, where an effective trophic level and can move quickly between harsher prey habitat
means one that interacts strongly). With ever-decreas- and more moderate conditions nearby (Louda, 1986,
894 B. A. MENGE ET AL.
Downloaded from https://academic.oup.com/icb/article/42/4/892/659154 by guest on 18 August 2022
FIG. 2. Predictions of CSMs and PSMs (after Menge and Olson, 1990). See text for further explanation.
1988; Menge and Olson, 1990; Louda and Collinge, but is insufficient to support more than sparse consum-
1992; Olson, 1992). With stress, prey devote the ma- er abundance (EFCL 1). With further increases in pro-
jority of their resources to stress responses and are ductivity, consumer abundance increases, and through
therefore relatively more susceptible to consumer pres- increased consumption intensity, offsets the increased
sure, again making EFCL 5 1. Under benign condi- basal species productivity, maintaining a constant bio-
tions, stress impacts are minimal, and both members mass of basal species (from EFCL 1 to 2; Fig. 3).
of the interacting pair can devote the majority of their This model thus predicts that with increased pro-
resources to biotic interactions. ductivity, both prey and their consumers will be in-
These alternative versions of the ESM make con- creasingly well off nutritionally. Ecological measures
trasting predictions regarding performance of the prey such as growth rate, feeding rate, and reproductive out-
in the presence and absence of consumers (Menge and put and physiological measures reflecting these rates
Olson, 1990; Fig. 2). In the CSM, consumer perfor- should therefore increase with increased productivity.
mance decreases more sharply than does prey perfor- Performance and temporal scale
mance with increasing stress (Fig. 2, left). When con-
sumer and prey coexist in harsh conditions, the effects In these models, ‘‘performance’’ typically refers to
of consumers on prey are weak because predators are readily measured characteristics such as feeding rate,
under severe stress and devote most of their time and growth, survival, or reproduction. All of these mea-
energy to survival (Fig. 2, left). In more benign por- sures, however, are relatively long-term integrative
tions of the environmental stress gradient, consumers measures that reflect an average physiological state.
occur under optimal physical and physiological con- Feeding rate, for example, might be expected to de-
ditions and can devote most of their time and energy cline if organisms experience stresses (e.g., thermal or
to prey capture and consumption (Fig. 2, left). desiccation) that impair cell, tissue and organ function,
In contrast, in the PSM, consumer performance de- and should increase again once conditions improve
creases less sharply than does prey performance with and sub-organismal repair is complete. Feeding rate
increasing stress (Fig. 2, right). When consumer and can also decline due to behavioral avoidance mecha-
prey coexist in harsh conditions, consumer effects on nisms, if possible, and if not, consumers may die under
prey are stronger than in benign conditions because persistent severe conditions. Growth should also slow
prey defenses are weakened. In more benign environ- or stop with stress as the organism’s cellular machin-
ments, prey defenses are stronger, making prey less ery devotes energy to protein repair or destruction, and
vulnerable to consumption. resume again with improved conditions. Under field
Nutrient/productivity models conditions, measures such as growth, feeding rate and
reproduction can often be quantified, although field de-
Here too we assume a simple two-level food chain, tection of changes in these measures can take months
with consumers and prey varying in biomass along a to years. Environments can change on many temporal
monotonically increasing gradient of productivity (Fig. scales, however, ranging down to seconds, minutes,
3). As envisioned by Oksanen et al. (1981), this model hours and days, and molecular and cellular responses
predicts, initially, that with increasing productivity, also tend to occur on these more rapid time scales.
basal species increase from 0 biomass at very low pro- Thus, growth or feeding performance in the field as
ductivity (EFCL 0), to sparse biomass (EFCL , 1), to necessarily measured over longer temporal scales has
the point where production is sufficient to support an no hope of pinpointing the short-term events that
abundant basal species level that competes for space, might be the critical events that generate the long-term
INTEGRATING ECOLOGY AND PHYSIOLOGY 895
average patterns that ecologists can quantify. Only
measures that can quantify organismal condition on
temporal scales relevant to those upon which sub-or-
ganismal changes occur can provide this level of in-
sight. Such measures can also provide a ‘‘common cur-
rency’’ with which to quantify organismal condition or
performance across taxa.
Complexities
We recognize that these simple models do not cap-
ture many important elements involved in community
dynamics. Species interactions within a trophic level,
for example, can modify these simple food chain pre-
dictions, sometimes dramatically (Abrams, 1993; Ro- Downloaded from https://academic.oup.com/icb/article/42/4/892/659154 by guest on 18 August 2022
semond et al., 1993). Incorporation of density can also
modify model predictions by introducing positive ef-
fects of species interactions (facilitation, associative
defenses) (Burnaford, 1997, 2001; Bruno and Bert-
ness, 2001). Despite the lack of detail in these models,
exploring the links between ecological performance
and sub-organismal processes is itself a complex issue.
We believe that starting with a simple scenario and
adding complexity and detail when appropriate seems
the most productive way to approach the problem.
TESTING THE MODELS:ENVIRONMENTAL STRESS
As summarized by Menge and Olson (1990), evi-
dence consistent with the assumptions and predictions
of ESMs and N/PMs was available for marine and
non-marine systems in the 1970s and 1980s. Since
then, considerable effort has been focused on testing
N/PMs, mostly in the context of top-down/bottom-up
theory (Menge, 2000). Less effort has been directed
towards specific tests of ESMs (Louda and Collinge,
1992; Leonard et al., 1999), although considerable ef-
fort has been focused on the organism-to-community
impacts of environmental stress (Louda and Collinge,
1992; Bertness and Leonard, 1997; Helmuth, 1998,
1999; Leonard et al., 1998; Bertness et al., 1999; Bru-
no and Bertness, 2001). Below, we present the results
of a study aimed at testing ESMs.
Study system
To test the simple ESM models outlined above, two
of us (BAM, AMO) carried out field experiments in FIG. 3. Nutrient/productivity model (simplified, after Menge and
1990–91 at Colin’s Cove on San Juan Island, Wash- Olson, 1990; Oksanen et al., 1981). As productivity increases, food
ington, USA. We evaluated two ‘‘model’’ consumer- chain length is predicted to increase (bottom panel). At EFCL , 1,
prey interactions. We examined whelk-barnacle inter- productivity is sufficient to support a sparse basal species level but
actions to test the predictions of the CSM with inter- insufficient to support consumers. With increased productivity, first
actors that fit the assumptions (consumer larger and basal species (EFCL 0 to ,1 to 1) then consumer species increase
in abundance (EFCL ,1 to 1 to 2), with first competition, then
more susceptible to stress than prey). Because an ear- consumer pressure regulating basal species abundance.
lier study of limpet-algal interactions (Olson, 1992)
produced results partially consistent with the PSM, we
also assessed a limpet-red algal interaction. In this and solar irradiance (high vs. lower mid-intertidal
study, we tested whether those results would hold if zone, sunny and shady sides of concrete blocks, re-
assumptions (consumers smaller than sheltering prey) spectively), (2) by providing artificial shade (small
were relaxed. opaque plastic ‘‘huts’’) fastened into a subset of the
In both whelk and limpet experiments, we manip- experimental units (Fig. 4). Additionally, weather var-
ulated stress levels in two ways: (1) by placing exper- ied in the San Juan Islands during our experiments,
imental units in microhabitats differing in inundation creating another contrast in stress conditions. Warm,
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