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Top-down versus bottom-up regulation
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Do we live in a largely top-down regulated world ?
KARL BANSE
University of Washington, School of Oceanography, Box 357940, Seattle, WA 98195-7940, USA
(Fax, 206-543-5073; Email, [email protected])
Based on a review of mostly recent literature for a public lecture, the question is discussed whether we live in a largely
“top-down” regulated world rather than one formed “bottom-up” by the resources for plant and animal growth. Of
course, the top-down mechanism is predicated by bottom-up production, especially by the plants. Examples for the
effects of grazing and predation for the land and the open sea, but including coral reefs, are discussed. The answer to
the question posed by the title is affirmative. Ecosystems altered by man and urgent needs for marine conservation are
briefly treated.
[Banse K 2007 Do we live in a largely top-down regulated world?
1.
J. Biosci. 32 791–796]
Introduction
This paper reviews the question whether, by and large,
we live in a “top-down” regulated world. Obviously, the
physics (climate, seasons, geology, in the sea also vertical
water movement) set the stage on which the organisms act.
Also, on land and in the sea, resources determine growth
and reproductive rates, which are driven for plants by light,
water, and nutrients (primarily, phosphorus and nitrogen)
and for animals by food (“bottom-up” control). The biomass
and species composition of plants and animals that we
see, however, tend to be greatly affected by grazing and
predation (top-down). Also discussed will be contemporary
shifts in ecosystems, which in the open sea are principally
due to fishing but less so to pollution or climate change.
Finally, the urgency of marine conservation will be noted.
The review of mostly recent literature is based on a 2006
public lecture at the Institute of Oceanography in Dona
Paula, Goa, entitled “Why is much of the land green, but
most of the open sea blue?” In a few paragraphs the talk
explained the colour difference, but then proceeded to show
that there is much more to the question posed by the title of
the lecture than meets the eye. How green is the land once
sufficiently benign climate, water, and nutrients are present?
Do competition and individual growth rates determine which
Keywords.
species dominate, or do grazing and predation losses? The
view that still prevails among students of plant biomass on
land and in the sea is that, to the first order, only the resources
need to be investigated for understanding the temporal
and spatial changes of biomass, species composition, and
animal body size and age structure. Instead, the losses from
grazing and, for animals, from predation (top-down effects)
need equally be studied. To keep the review short, only the
deep-blue open ocean is juxtaposed with the land, with the
exception of coral reefs in the former, and the determinants
of biomass are mentioned only in passing.
2.
Hypotheses about the maintenance of a green world
While substantial discussion of the mechanisms limiting
the size of natural populations and the maintenance of the
specific composition during the past century goes back to
at least the 1930s, the current debate started with the “green
world hypothesis” of Hairston et al (1960), “Community
structure, population control, and competition” (see also
Slobodkin et al 1967). Addressing mostly terrestrial
patterns, and there, using mostly examples of plant-insect
interactions, they posited that (i) land plants are limited by
resources for which they compete, while the other trophic
levels (herbivores, carnivores, and decomposers) are subject
Bottom-up; coral reefs; conservation; Land vs sea; overfishing; top-down
http://www.ias.ac.in/jbiosci
J. Biosci. 32(4), June 2007, 791–796, © Indian Academy
Sciences
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Karl Banse
to different mechanisms of control (see below). (ii) Plants
are generally abundant and intact. (iii) Herbivores (the term
was restricted to consumers of vegetation, but excluded
seed eaters, which tend to be omnivores) can deplete plants,
especially when the herbivores become numerous because
of being protected from their predators by, e.g. man. (iv)
Herbivore populations, instead of being limited by food
(the resource), are normally reduced by their predators and
parasites, and for this reason do not consume all the plants,
and the world remains green. (v) In turn, the predators as
a trophic level reduce their own food supply and have
to compete with each other; there is much less food per
carnivore than there is per herbivore.
The strong alternative explanation for the maintenance
of the green world as reviewed by Polis (1999; see also
Worm et al 2002) is that the herbivores indeed do not
eat all plant matter, but largely because it is indigestible
structural material (cellulose and lignin) or because of plant
defenses. The defenses are principally chemical compounds,
which make leaves and juices unpalatable or poisonous.
Also, herbivores may not achieve optimal growth nor high
abundance because of nutritional inadequacy of the food.
Since the 1960s, discussions and field manipulations
have yielded further insights. Communities of long-lived
trees and mammals do not lend themselves easily to
experiments, while in the sea, bottom assemblages with the
shorter lifetimes of dominant species proved to be excellent
objects (Paine 2000). As on land, unchecked grazers can
create almost barren rock also in the sea, and benthic algae
during individual growth may reduce grazing loss by virtue
of attaining large size, like trees. Generally, however,
herbivores determine the biomass and composition of the
algal assemblages, while competition (here principally for
space) and chemical defenses are insufficient to provide
dominance by themselves.
A large, community-wide terrestrial experiment testing
the green world hypothesis was created by a hydroelectric project in eastern Venezuela, approximately at
the (southern) latitude of the southern tip of India. Since
1986 the reservoir covers an area slightly larger than the
entire state of Goa. From 1990 to 2003, twelve islands of
variable size covered by dry forest and initially with the
original but now trapped animal populations were studied
(Terborgh et al 2006). Numbers and kinds of tagged trees,
new saplings, and animals were tested. As expected, the
persistence of animal species was highly correlated with
island size, such that predators of vertebrates disappeared
quickly from the medium- and small-sized islands (4–11
ha and 0.6–1.5 ha, respectively) due to insufficient prey.
On the small islands in 2001/2002, in consequence, some
vertebrate and invertebrate herbivores including leaf-cutter
ants were up to two orders of magnitude more abundant than
in the controls (large islands and the mainland); nearly every
J. Biosci. 32(4), June 2007
plant species was negatively affected; the understory of the
forest had vanished; several of the grown trees had died; and
perhaps most importantly, the number of new saplings had
declined to 25% of the controls, apparently mainly due to
the ants. In sum, the small islands were clearly overgrazed.
The final situation appears to be islands nearly without live
trees but covered by fallen trees overgrown by herbivoreresistant lianas. The conclusion of the study is that a viable
predator guild is required to maintain the diversity of the
entire community, and that there is top-down control of the
herbivores as claimed by Hairston et al (1960).
Paine (2000) suggested that including large-bodied
herbivores (e.g. bison, elephant, hippopotamus) alters
the conclusions by Hairston et al (1960) somewhat. He
noted that these animals differ from smaller ones by not
only consuming plants but breaking or trampling them
and changing the landscape. Jackson (1997) pointed out
the same for large marine turtles and manatees/dugongs.
Removal of such grazers, i.e. of the top-down control
mechanism, changes the plant species composition
drastically. Moreover, removal may help alter the herbivore
communities indirectly through competition because those
grazers may sometimes be food-limited. On land, the
green colour, of course, persists. Keep in mind, though, the
review by Polis (1999): the various control mechanisms
maintaining the green world normally do not operate singly,
but the relative effects certainly vary (see also Leibold et al
1997 and Menge 2000). The question is which mechanism
predominates more frequently on which spatial and temporal
scales.
The biology of the blue open sea differs in several
respects from the terrestrial realm. For example, because of
the high density of water, the unicellular phytoplankton cells
do not need elaborate physical supporting structure, they
drift freely, and each individual usually divides every few
days. Although the cells are all microscopically small, the
weight range corresponding to the average size of 1–100 µm
is about one million, similarly to that between voles or small
mice and elephants; both size ranges cannot be caught by
one net or mouth, so there is always size-related grazing and
predation. The cells tend to be eaten wholesale; here is no
insect nibbling on a tree. Most cells are consumed within the
day they have divided, and the nutrients in the newly formed
organic matter are recycled into the water for use again,
bottom-up resulting from top-down. A semi-steady state or
balance of concentrations is usually maintained for months
in large regions of the open sea. As noted by Banse (2002),
the cause for the actual chlorophyll and biomass values (why
are they not 1/3 or 3 times the observed averages?) is not
understood. Gradually, gravity removes particulate organic
matter with the associated nutrients to the dark interior,
resulting in the low nutrient content of the sun-lit zone and, in
turn, the low number of living and dead particles. Therefore,
Top-down versus bottom-up regulation
the ocean color approaches the deep blue of pure water. On
large spatial (basin-wide) or temporal (seasonal) scales,
higher nutrient supply from physical processes supports
higher chlorophyll and meso-zooplankton (millimeter size)
concentrations, as well as larger fisheries yields (bottom-up,
Ware and Thomson 2005 for a spatial example). As stated in
the Introduction, the physics are setting the stage.
Ocean-wide, only rarely does the phytoplankton biomass
accumulate into “blooms” even after nutrients became
available in large quantities from physical forcing. In three
blooms of the open sea that were revisited, so that mortality
could be determined, the loss from grazing by the time of
the phytoplankton peak was more than one-half to almost all
of the cumulative production (Banse 2002). In consequence,
the rate of population increase was much smaller than the
rate of cell division. Thus, even bloom dynamics clearly
initiated by bottom-up processes cannot be understood by
studying only the resources, i.e. nutrients, underwater light,
etc. (For chemical defenses against grazing in freshwater
plankton, see van Donk 2005.) In summary, the biomass of
plankton is greatly affected by top-down control, as is the
species composition because of size-selective grazing or
predation, but it is unclear how “green” the sea is given a
certain flux of resources.
3.
Removal of predators by man
On much of the land originally forested after the ice age,
some 10,000–12,000 years ago, and on the primeval
grasslands not only has much of the original community
vanished first from hunting and then through agriculture,
but also in the remaining semi-wild regions, the predators
have been reduced or exterminated, as is true in the sea.
For instance, since this paper is based on a lecture in India,
lions used to live in ancient Greece (cf. the Lion Gate at
Mykene) and Mesopotamia (cf. the depictions of Assyrian
rulers hunting lions from horseback at Niniveh), and the
State seal of India depicts a lion capital from a column of
Ashoka’s time. Now in India, about 300 lions are left in
the wild and only in the Sasan-Gir National Park, Gujarat
(see “lion”, Wikipedia, The Free Encyclopedia). Similarly,
elephants and rhinoceros used to be widespread in Africa
and Asia, but their abundance has been greatly reduced.
Again in India, the numbers of the largest cat, the Bengal
tiger, are in serious decline. A century ago there were about
40,000 specimens (the reference cited below does not state
whether the number refers to the entire Indian Peninsula
or today’s India) but presently, the Indian government
estimates the number to be 3,600 (likewise from Wikipedia,
as cited) while knowledgeable observers believe it to range
between 1,200 and 2,000 (Check 2006). The current threat to
the tigers appears to be not so much from poaching on them,
but from fragmentation and disappearance of habitat for the
793
large hoofed herbivores, the tigers’ prey, and poaching on
these (Dalton 2006). This is a bottom-up effect for the cats.
The man-made reduction or absence also of other
terrestrial carnivorous mammals, reptiles, and raptors among
birds, by hunting, loss of habitat, or reduced reproduction
because of insufficient prey relieves the predation pressure
on the medium-sized grazers. The decreased top-down
effect then can greatly alter the dominance among the
vegetation or, unless herbivores are being culled, may lead
to overgrazing. Goats, which feed on the above-ground plant
matter including the saplings of trees, but do not disturb the
roots as many of the larger grazers do, are widely distributed.
The goats, together with frequent burning over the millennia
around much of the Mediterranean Sea, have transformed
forests on dry, rocky grounds into the very dense macchia
or thicket-shrubland, or elsewhere into grassy semi-deserts.
When the top-down control by goats in such climates
is removed from otherwise unused land, native plants
including trees return, as, for example, in Israel’s Negev,
which after 1982 was fenced off from the Sinai Peninsula to
the west (Meir and Tsoar 1996; sheep and camels were also
excluded), or on some of the equatorial Galápagos Islands
(Guo 2006). Another, grandiose example for the effects of
an unchecked herbivore was the introduction of rabbits to
Australia. Already before that, rabbits not under effective
predator control in many parts of England were among the
most important agents for the nature and direction of plant
succession (Elton 1927: chapter 5; recent references in Paine
2000).
In the low-latitude open ocean, the big “top”-predators are
sharks, adult large fishes, and squids, besides some toothed
whales and sea birds, and are essentially all piscivores. At
higher latitudes, large fishes like cod-relatives step in. The
prey of the top-predators may likewise be piscivorous or
be consumers of the invertebrate “grazers”, i.e. suspension
feeders, which are eating the very small zooplankton and the
phytoplankton. Top-down effects will act. Note that natural
predation differs from fishing. Many species are restricted to
a few kinds of prey, and in any case, all terminate hunting for
the preferred food and switch to different prey when the yield
falls below the level needed to pay for the metabolic needs.
In contrast, for fishermen the prize realized for rare prey
tends to go up when catches fall, and anyway, the pervasive
fuel and other subsidies distort the balance between expense
and income, i.e. they permit the continuation of exploitation
beyond the money received for the catch itself, and the
reduction of abundance well below that caused by natural
predation.
The technological advances after World War II
introduced long-distance fisheries, so that even open-sea
populations of sharks and large (meter-long and larger) fish
were drastically reduced. For example, Japanese longline
fishing, reported uniformly for the three oceans, showed
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Karl Banse
that in the entire Indian Ocean north of 45˚S, 8–10 hooks
per 100 hooks caught tuna, billfishes, and swordfish in the
mid-1950s (sharks not recorded). The catch for the large
specimens declined exponentially to 1–2 per 100 hooks by
2000, similarly as in the other oceans (Myers and Worm
2003; longlines are kilometer-long lines from which several
hundred or even one thousand baited hooks dangle and which
are trolled each for a few hours; the method is not recent
but the modern boats now can routinely operate far from
land). Over the same period, the mean maximum length of
landed fishes and invertebrates diminished in large regions
of the open sea by > 0.5 to > 1 m (Jackson et al 2001; Pauly
et al 2005). The larger specimens within each species are the
older ones and their replacement takes more time than that
of the younger individuals, so that the age composition of an
exploited population is truncated by fishing; smaller females
of a species spawn fewer eggs than large ones. Polacheck
(2006), by means of Indian Ocean data as the example,
criticized Meyers and Worm’s (2003) use of catch figures
as the measure of population biomass, which led to great
overestimates of the decline of populations.
The quantitative effects on the food web of reduced body
size and population biomass of the top predators on the
immediate prey, as well as the prey’s food, are at present
surmised for the open ocean (e.g. Myers and Worm 2005;
Essington et al 2006). The quantitative understanding is
severely hampered by the concurrent high fishing pressure
exerted on the prey of the top predators, e.g. the herring. For
the last 1–2 decades, the effects on the food webs of the open
sea have been of great scientific concern, after overfishing
(i.e. taking more of a species than can be replaced by
growth) in coastal seas and over the continental shelves
became apparent many decades ago. It was shown to have
occurred in the (coastal!) North Sea and some Caribbean
reefs for at least two centuries, so that the biomass and
species composition are not the original ones (Jackson 1997).
Globally speaking, fishing is the major modifier of pelagic
food webs, while pollution and other man-made effects are
subsidiary (Jackson et al 2001; Pauly and Maclean 2003).
The result of removing the top levels of the food web
is actually visible to the naked eye in the coral reefs of
those blue oceans. In almost a caricature of the pristine
setting, hungry sharks are on top of the food web, which
feed on large piscivores like groupers and seals. These in
turn prey heavily on the numerous and varied herbivorous
fishes, which prevent the benthic algae from overgrowing
the slowly-augmenting corals. With the top predators and
other large piscivores, as well as many herbivorous fish
removed by fishermen, collectors of aquarium species, and
spear-hunting tourists, many reefs near population centers,
especially those served by airports, have turned green-brown
from leafy algae during the last 1–2 decades. The coral
structure of many reefs is hardly visible any more and decays
J. Biosci. 32(4), June 2007
because the physical structure of most of a reef is fragile and
the corals need light for growth (Jackson et al 2001). Coral
bleaching by episodes of warming does not help, and there
are few atolls and fringing reefs left in the entire world that
still harbour sharks, seals, and meter-long groupers.
Globally, a 2004 report based on a 1997 comprehensive
survey (Hodgson 1999) estimates that 20% of the world’s
coral reefs (not including deep-water corals) had effectively
been destroyed since ≥ 90% of the corals are lost,
approximately 24% are at imminent risk, and another 26%
are threatened (Wilkinson 2006). Even the huge Australian
Great Barrier Reef is affected but recently, a full 33% of it
has been declared as no-take zones (no fishing, no coral rock
mining, etc.; Knowlton 2006).
4.
Urgency of marine conservation
In the pelagic zone of the subtropics and higher latitudes
of the North Atlantic, no extensive pristine environments
remain (Pauly and Maclean 2003; see Jackson 2001 for
the western North Atlantic). As indicated, with the many
long-distance fishing fleets working in the open sea of all
oceans, overfishing is common worldwide. By 2003, for 5/6
of the global catch, 3/10 (29%) of the fished species yielded
≤ 1/10 of the highest catches recorded since 1950 (Worm
et al 2006), which in many regions was long after the onset
of intensive fishing. Also, the world’s marine catch appears
to have been more or less stable since the late 1980s after
having steeply increased since about 1950; catches per unit
effort are declining worldwide (Pauly 1996; Pauly et al
2005).
Among the reasons for overfishing are the usual
unwillingness of fishermen to accept catch limits, especially
where fishing is the only source of income; the attraction
of the short-term gain compared with the delayed benefits
of conservation; the need to amortize the investment in
new boats in an often over-capitalized business; in view
of the resulting social costs (e.g. unemployment, the
associated compensation, re-training), the reluctance of
governments to accept, set, and enforce the low catch limits
recommended by scientists; by the time a government does
accept recommendations, years may have passed and a
more stringent limitation would be needed. In hindsight, the
majority of accepted catch limits have often been too little,
as well as too late.
Major needs for action were outlined by Pauly and
Maclean (2003: chapter 4) and Hilborn et al (2003), as
two of many voices. They note the necessity for greatly
reduced fishing effort for many species, individual catch
quotas, marine reserves, transformation of the market by,
e.g. reducing the subsidies, and alteration of governance.
Hilborn et al (2003) remarked that fishing is normally an
economic activity, but most efforts so far have been directed
Top-down versus bottom-up regulation
at the biological side of restoring stocks. Regarding marine
reserves, Pauly and Maclean (2003: 118) suggested that at
least 1/5 of the ocean should be protected by 2020. These
reserves (also called Marine Protected Areas) are meant to be
permanently closed to fishing. That may not only bring back
fish populations but help toward restoring the ecosystems.
Hilborn et al (2003) appear to be more conservative in
their specific suggestions. Anyway, because of the present
state of the seas, “Conservation is a necessity, not a
luxury” (Roberts et al 2006, in the context of coral reefs).
Fortunately, worldwide and in contrast to the land, only a few
of the originally present species have become truly extinct
although many may have vanished in parts of the original
area of occurrence. It remains to be seen, though, whether
the majority of fish species brought down to really small
populations will recover (Hutchings and Reynolds 2004).
All of the above will require sacrifices by groups of current
users and adequate compensation for losses. Therefore, the
needed solutions are as much a socio-economic issue as one
of scientific research. One difficulty here is that largely it has
not yet been possible to objectively weigh economic costs
and benefits of, e.g. conservation of an entire atoll based
on no-catch versus the income from later ecotourism (large
cohesive areas are needed for restoring and maintaining
sharks and other top predators at a reef). However, we do not
have many decades to lose before active conservation has to
be in place in many regions (e.g. the citations to R Hilborn, J
B C Jackson, D Pauly, and their colleagues). We can neither
continue for very long the current industrial fishing practices
in the open sea, which are based on free access, nor the
over-utilization of coral reefs from subsistence fishing and
unchecked tourism. The major impediment to large-scale
change in most countries is lack of political will vis-à-vis
actual needs for income by fishers or pressure by industry.
The voters at large have not yet grasped the necessity to
request wise management of common-property resources
from their governments.
Because of the site of my lecture in Goa, I return once
more to India. There is a need for action also here. Principally
on the continental shelf, the development of her fisheries in
the last half-century by mechanization of indigenous boats,
construction of new and larger vessels, large government
subsidies, increasing demand for seafood, and a concurrent
raise in market prices, have led to a harvesting capability that
exceeds the estimated sustainability of most of the exploited
species. Many populations are overfished. The catch per unit
of effort has decreased markedly, which is a sure sign of a
large decrease of abundance, and fishing mortality exceeds
natural mortality (Devaraj and Vivekanandan 1999).
There are too many boats. Yet, the government subsidies
in the broadest sense for fisheries in India, including, e.g.
construction or renovation of fishing harbors and boats,
research, storage infrastructure programs, tax exemption,
795
surveillance, etc., in 2000 exceeded the landed value of
marine fish by 123%, not including fuel subsidies (Sumaila
and Pauly 2006: Appendices I and II). To protect juvenile
fishes and prawns, hook and mesh sizes are now being
regulated, and the states along the southwest coast have
closed fisheries during the southwest monsoon for 30-90
days, principally to guard prawns during the spawning
season. During this time, the fishermen are without income
and so far, no compensation is being paid, which is the
custom in the countries surrounding the North Atlantic.
In my lecture I ended on quite a pessimistic note, saying
that in India the political will to institute countrywide
ecologically adequate conservation, for land and sea, may
not be generated for about two decades even if the subject
was introduced in elementary schools right away. Unless a
sufficiently large fraction of the then-voting population is
educated about the issues, it will be difficult to mobilize the
political will sufficient for major change.
5.
Conclusion
In summary, worldwide under sufficiently benign conditions,
the terrestrial stage on which the organisms act is mostly
green. However, the numbers or biomass and the types or
species of the actors are largely top-down regulated. The
open sea is nutrient poor, hence supports little biomass and is
blue but again, the types of organisms are heavily regulated
top-down, as holds also for the coral reefs. Several examples
were chosen for the Indian audience, but the underlying
mechanisms act worldwide.
Acknowledgements
The travel to Goa was made possible by an invitation to a
workshop supported by the US National Science Foundation
(Office of International Science and Engineering) Grant
No OISE-0536861, PIs, R R Hood and S W A Naqvi.
The National Institute of Oceanography of India offered
great hospitality during the visit. The writing was partially
supported by TIAA/CREF and my Grant No N00014-041-0142 from the US Office of Naval Research. B W Frost
suggested improvements to the presentation and recent
references, and two anonymous reviewers made useful
suggestions. I owe many thanks to all.
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MS received 29 January 2007; accepted 14 May 2007
ePublication: 15 May 2007
Corresponding editor: VIDYANAND NANJUNDIAH
J. Biosci. 32(4), June 2007