FOOD WEBS 259

be an important factor in the patterns of species diversity that we observe in communities.

Fire, storms, and human actions are all disturbance forces that alter the existing structure
and/or physical environment of a community or ecosystem, leading to new colonization
opportunities. Disturbance is an event that causes the death, displacement, or harm to
individuals within a population, community, or ecosystem and leads to opportunities for
new individuals to replace them.
Hurricanes represent large-scale disturbance events. Yannarell et al. (2007) used the
occurrence of Hurricane Frances, a category 4 storm, as a natural experiment to study
the effects of disturbance on cyanobacterial mats on San Salvador. This mat community
appeared to be in an equilibrium state before the hurricane, and changes in community
composition and salinity in the equilibrium state did not change some ecosystem parame-
ters, such as the C : N ratio. Hurricane Frances, however, greatly lowered salinity values
and deposited layers of sand on the cyanobacterial mat communities, leading to dramatic
shifts in community composition and C : N ratios, pushing them out of equilibrium.
Dominant cyanobacterial species decreased, and more rare species existing prior to the
hurricane, increased substantially in proportion. Despite the shift of the community from
equilibrium, the community rapidly recovered. Perhaps the most important conclusion
of this study is the support for the hypothesis that more diverse communities are better
able to recover from massive disturbance, due to redundancy in function of community
members. Thus, previously rarer species may take over ecosystem functions such as
nitrogen fixation following major disturbances. This was seen in the study by Yeager
et al. (2005) of the effects of a major fire on community composition of nitrogen fixers
and ammonia oxidizers. Thus, redundancy contributes to ecosystem resilience. But what
about intermediate levels of disturbance?
Disturbance can affect social traits such as cooperation and supports the contention
that disturbance leads to coexistence. Brockhurst et al. (2007) suggested that cooperation
can only evolve in situations in which disturbance is moderate. At low disturbance rates,
although cell densities reach critical levels for cooperation to be beneficial, cheaters arise
and gain a selective advantage, eventually dominating the population. At high disturbance
rates cheaters predominate because mass mortality events prevent cell density from reach-
ing a level in which cooperation is beneficial. This study dovetails with the more general
hypothesis that intermediate levels of disturbance lead to greater diversity (Buckling
et al. 2000), referred to as the intermediate disturbance hypothesis [IDH (Figure 9.7),
proposed by Joseph Connell in the mid-1970s]. Moderate levels of disturbance facilitate
higher species diversity due to tradeoffs between competition (competitive exclusion)
and colonization. Many studies have failed to support IDH, leading Cadotte (2007) to
examine the tradeoffs between competition and colonization at different scales. Cadotte
showed that where species are on a gradient of colonization/competition, the resulting
diversity is affected; differing levels of disturbance create a gradient of colonizers, while
a gradient of time since disturbance creates a gradient of competition. He also showed
that scale matters, demonstrating that the IDH holds at larger scales than the local patch.
Type, frequency, and level of disturbance strongly affect community species diversity,
but we still have much to learn about exactly how.

9.9 FOOD WEBS

A food chain is a representation of the flow of energy within a food web, from one to
level to the next, showing the sequence of what is eaten by what. A food web represents
feeding relationships within a community and linkages among food chains. Food chains
260 LIVING TOGETHER: MICROBIAL COMMUNITIES

Addition
of nutrient A Multinutrient
and nutrient B Co-limitation
increases growth

Biochemical
Resource Co-limitation:
Co-limitation Single species
responds to
either nutrient
A or B
Either nutrient A
or nutrient B
increases growth Community
Co-limitation:
Different species
respond to
either nutrient
A or B

Figure 9.8. Replacing the more traditional view that one nutrient usually limits a population,
new evidence now suggests that multiple nutrients limit organisms and even communities in
several different ways as shown here [modified from Arrigo (2005)].

and food webs are important constructs in ecology. The author can still remember the
excitement of the speaker at the Woods Hole Microbial Diversity course in 1993 as
he introduced the idea of the widespread nature of picoplankton, a newly discovered
component of the food web in Earth’s oceans. Little did we know then how important
the many yet to be discovered groups of microorganisms are in food webs. In fact, few
studies even incorporated microorganisms into food web investigations.
Microorganisms represent important components of food webs (Section 4.4.1), and
are depicted as the base of most food webs. Much of the ocean is occupied by photo-
synthetic microorganisms (Cyanobacteria and algae), Archaea, protozoans, and viruses
whose diversity is just being uncovered (see also Section 4.3.2). Protozoans prey on the
various bacterial components of the food web, limiting bacterial population sizes; those
microorganisms that escape predation may fall victim to pathogenic viruses (Smetacek
2002). A few studies have examined predominately microorganisms in soil food webs
(see Section 4.4.1) and microbial food webs or have constructed microcosms to study
microbial food webs.

9.9.1 Structure of Microbial Food Webs

What affects the composition of food webs? Predation (top–down effect) and the avail-
ability of resources (bottom–up effect) can potentially affect species diversity within
microbial communities. Yet, how does diversity within trophic levels affect how resource
availability and predation effects are felt throughout the food web? Fox (2007) set up
microcosm studies with bacteria as the resource base and different schemes of protist
prey, and predators, varying from depauperate food webs to several levels of prey in a
food web. He found that as he increased productivity in his systems, prey and predator
biomass increased (bottom–up effects); if predators were present, prey biomass decreased
and changed in composition, which, in turn, led to an increase in the bacterial resource
base [top–down effects (Fox 2007)]. Now let’s add another wrinkle to the discussion.
What happens when the environment is more extreme, lowering diversity and possibly
eliminating or decreasing top–down predation effects?
PRIMARY PRODUCTION AND ENERGY FLOW 261

Microorganisms exist in a wide range of environmental conditions, including condi-

tions of pH, temperature, and pressure that humans and other organisms consider extreme.
These extreme conditions may result in lower species diversity and the absence of top
predators and certain functional groups within the food web, but the full complexity
of how extreme conditions affect food webs and food chains is still under study. By
contrasting and comparing two acidic lakes (pH ≤ 3), which are species-poor with two
neutral lakes of different productivities, Gaedke and Kamjunke (2006) were able to tease
apart some of the effects of acidity and trophic state. The four lakes they chose differed
in size, which did not seem to be a factor in the differences in food webs. Productivity
differed markedly between the two neutral lakes. In the two acidic lakes, the third and
fourth trophic levels were missing, but this was not attributed to productivity. Acidity
clearly affected species richness (lower in the acidic lakes), the degree to which different
functional groups were present, and the composition of consumers. However, the ratio of
heterotrophs to autotrophs appeared to be more dependent on the degree to which a lake
was oligotrophic to eutrophic (trophic state). Thus, in those lakes that are dominated by
microorganisms to differing degrees, we can see that environmental stressors such as pH
can affect the food web structure.

9.9.2 Keystone Species Effects on Food Webs and Diversity

The concept of keystone species was proposed in the 1960s by Robert Paine and suggests
that predators can have profound effects on species diversity by keeping prey below their
carrying capacity (Molles 2008). When prey species are kept below their carrying capac-
ity, they do not competitively exclude their competitors, thus leading to increased species
diversity. Because of their position in the food web, bacteria rarely function as predators,
but are more often prey and therefore unlikely to function as keystone species. However,
as a group, one might argue that they are limiting the carrying capacity of humans. Other
microorganisms, including fungi and protists, function as predators within food webs.

9.10 PRIMARY PRODUCTION AND ENERGY FLOW

9.10.1 Cycling of Nutrients

Marine microorganisms are responsible for roughly half of Earth’s primary production
(Arrigo 2005)—that’s a stunning statement! If we want to understand nutrient cycling,
these are key organisms and communities to study. Marine phytoplankton include the
microscopic algae and diatoms that float in the ocean and are responsible for the bulk
of marine photosynthesis. Marine phytoplankton strongly influence the availability of
nutrients in the oceans, and we are influencing these organisms and communities through
anthropogenic activities such as nitrogen runoff into the oceans. The microorganisms
shape nutrient availability and are, in turn, shaped by what nutrients are available. New
discoveries since the 1990s have shown that these organisms and communities may be
limited by multiple nutrients. Let’s take a look at some of the complexities of this system,
which is only now beginning to be understood.
Our oceans show a ratio of 16 : 1 of nitrogen to phosphorus, which corresponds to the
average ratio seen in marine phytoplankton; this is called the Redfield ratio. Overall, our