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Trophic uncertainty vs parsimony in food web research

Debal Deb, WWF-India, Eastern Region, Tata Centre 5th floor, 43 Chowringhee Rd, Calcutta 700071, India.

Gut content analysis (GCA) is the most widely accepted method
for generalising about a species' food habits. GCA is valuable if
the purpose of the study is to determine the frequency or strength
of interactions between species, or to establish new food links.
However, determining all food links through GCA is impossible
for large speciose webs. Furthermore, GCA may not reveal the
true nature of linkage dynamics due to environmental and
physiological stochasticity. It is therefore parsimonious to as-
sume that linkages between species recorded in the literature will
be found in all food webs, if the same prey and predator species
occur in those systems.
To reveal new linkages, fresh GCA is desirable, but impracticable
for large speciose webs containing many rare and endangered
species, in which case it may be replaced by several non-dissective
methods. High-resolution data for tropical webs could be gener-
ated through observations made by trained indigenous peoples.
tions. This, combined with the fact that different non-
dissective methods have been employed by food web
researchers only in recent years (e.g. Havens et al.
1996), seems to indicate that GCA has been held by
many authorities to be the most reliable method.
Schoenly and Cohen (1991), for example, insist that
GCA is indispensable for establishing food linkages,
and ought to be conducted afresh for every new de-
scription of a food web, in order to ascertain the
trophic links actually existing in the system during each
period of observation.

Gut content analysis (GCA) is performed to find out
what an animal has eaten, and the finding is subse-
quently generalized: what has been found in a speci-
men's stomach would represent the diet items of the
species. This kind of inductive generalization is a pow-
erful tool in biology. However, inferring from GCA
may not always reveal the true nature of interaction
dynamics (Stoner and Zimmerman 1988). For example,
the variety and density of prey, access to the food
items, predator hunger and gustatory preferences may
affect the inferences drawn from the typological GCA.
Not only are the trophic links always in a state of flux
(Lane 1985), but the directionality of the links also
varies according to developmental stages of organisms
(Warren 1989, Deb 1995). Thus, the gut contents of
today's samples are likely to differ from those of an-
other time; similar samples from different communities
may also yield different GCA results, due to their
different species compositions and abundances, and
also perhaps due to different environmental influences.
Considering these and other limitations of GCA,
many researchers have adopted several alternative
methods, but their explanations as to why GCA was
not conducted (Stoner and Zimmerman 1988, Havens
1991, Polis 1991, Deb 1995) often appear to reveal that
peer review of such works demanded those explana-
Trophic indeterminateness
Precision of inferences regarding the structure of a food
web crucially depends on the resolution of data. To
describe an entire web requires identifying all taxa in
the system, which appears too ambitious to accomplish.
The checklist of species in a moderately sized commu-
nity tends to lengthen with time and effort spent on
identifying them (Cohen et al. 1993, Havens et al.
1996). As a corollary, the diet spectrum of anyone
species is likely to increase indefinitely with efforts to
discover them (Polis 1991). One might call this "trophic
indeterminateness", which seems to be corroborated by
a growing body of evidence.
Polis (1991) derived his "species-effort curve" from
his study of desert arthropods, and aquatic systems
have also yielded similar results. For example, the
water flea Daphnia, known to be purely herbivorous,
were reported by Gilbert and coworkers (Burns and
Gilbert 1986, Gilbert and MacIsaac 1989) to kill and
consume small rotifers such as Keratella in the process
of filtering algae. Calanoid copepods, known as pelagic
herbivores, are now reported also to eat small bra-
chionid rotifers (Warren and Lawton 1987). Until re-
cently, phagotrophic uptake of bacteria by phyto-
flagellates (Tranvik et al. 1989) was also unknown.
Aquatic micro-organisms await intensive studies to re-
veal further det.ails of feeding behaviour. Terrestrial
examples include such common mammalian herbivores

OIKOS 78:1 (1997) 191

as sheep and red deer who occasionally consume
live birds - to meet mineral deficiencyin food (Bazely time-specific ~ebs, constructed "by assuming that a
1989), and the Arabian wolf (Canis lupus arabs) in the
Sarawat mountain range who thrive mainly on fish and
birds, as reported in the March 1995 issue of BBC
Wildlife reports (p. 11). Thus, the number of potential
food items of an animal may be larger than what is
believed to be its actual diet spectrum. By contrast, a
potential food organism may not be eaten by the
predator, if the prey has anti-predator adaptations: for
example, Keratella slacki, Brachionus calyciflorus, and
Polyarthra spp. most effectively evade predation from
the predatory rotifer Asplanchna (Kerfoot and Sih 1987,
Gilbert and Kirk 1988).
In spite of this expanded knowledge of feeding biolo-
gies, the presence or absence of the trophic links may
not always be detectable by random gut examinations
due to stochastic environmental and physiological rea-
sons. Predator hunger, for instance, regulates the
planktonic clearance rates of both usually-resistant and
susceptible prey (Stemberger 1985). Furthermore, a
fresh GCA may reveal that a particular resource type is
absent from the gut of an animal, but that may not
indicate the "absence of a link. Rather, it simply means
that the predator did not eat the prey type during the
period equal to the gut passage time", when it was
examined (Havens 1991). Such spatio-tempora1 uncer-
tainty about the constancy of dietary links may debili-
tate the very objective of GCA.
Schoener (1989) opined that the decision to draw
potential links must be either "vetted by experiments ...
or by extensive comparative observations, both hard to
come by and unlikely to be obtained for most food
webs in even the far future, however desirable" (p.
1586). Schoenly and Cohen (1991), however, not only
demand such experiments and repeated observations be
performed, but would also like to see the ideal student
to report the fluctuations of population densities, as
well as seasonal changes of selected abiotic environmen-
tal parameters. that might give clues to the flux of
dietary links. Thus, they suggest that trophic linkages
be 4educed from all empirical data in every particular
case, instead of inducing them from a few cases. This
stand is characteristic of extreme empiricism, and leaves
no scope for generalization. One may also argue that
Schoenly and Cohen's recommendation implies that
first we describe a phenomenon (here, presence/absence
of trophic link), and then seek a suitable cause (e.g.
_environmental parameters) by reference to which we
can explainthe phenomenon under that description - a
procedure that corrupts the scientific method.
Application of Occam's razor
In contrast with their own recommendation, Schoenly
and Cohen (1991) themselves relied on the published
192
data of food habits of the species comprising their
feeding link from prey A to predator B was present if
and only if such a link was present in the cumulative
web and species A and B occurred together at the time
of observation". A cumulative web is a web which
incorporates all known trophic links between pairs of
species across time (links during summer, winter, day
and night, for example). Thus A is assumed to be
linked always to B, regardless of how often A eats B, or
whether this link is stronger or weaker than other such
links in the community. This parsimony of assumption
that the links between pairs of (onto)species observed in
the past will be observed in the future and in similar
systems involves application of Occam's razor, which is
essential for all rational enquiry (Lindh 1993). Based.
essentially on this argument, most recent food web
studies are literature-dependent, and yet show improved
generalisations about web statistics (e.g. Martinez 1991,
1992, Havens 1992, 1993, Deb 1995). The essential
improvement in these studies has been due to finer
resolution of known data rather than using new dietary
information.
One problem with cumulative webs is that if ontoge-
netic diet shifts occurred, the simultaneous presence of
A and B in their webs would not necessarily signify a
feeding relation between them (Schoenly and Cohen
1991). Thus, if B is eaten by the juvenile, but not
the adult of species A, the calculation of food links
between them whenever A and B co-occur would
simply overestimate the number of actual links in
cumulative webs. This overestimation could be avoided
if the relevant life-history stages of organisms are de-
scribed separately as distinct web elements in the cumu-
lative webs (Havens 1992, Deb 1995). I would like
to call such elements ontospecies (Deb 1995). Thus,
species A may be resolved into onto species X (the
young of species A) and Y (adult A), such that B
(in the above example) is linked with X, but not with
y.
Estimating overestimation limits
Constructing cumulative webs implies that the organ-
isms"in the web under study use (or, will use) all trophic
biologies they are known to use. As a result, the
number of food links (L) tends to be overestimated
(Pimm et at. 1991). Here the methodological problem is
whether the overestimation of L approximates the to-
pologically maximum number of feasible links (Lmax)
amongst all onto species, in which case the whole exer-
cise of cumulative web analysis is bound to yield spuri-
ous results. Lmaxis defined as
Lmax = [S(S - If- I Si(Si - I)J/2 = I SiCS - sJ/2,
OIKOS 78:1 (1997)
where s; is the number of species on the ith trophic
level, and S = L s;. To test if L calculated from cumula-
tive webs might approximate LmaX' I analysed my own
data on two freshwater ponds from southern Bengal,
and simulated 11 500 randomized webs on computer,
using the same pool of onto species (Deb 1995). All
trophic links between the onto species were inferred
from the literature. The result (Fig. 1) shows that the
two estimates move increasingly apart from each other
as S increases, and the lower limit of the Lmax range is
above the upper limit of the range of L. This indicates
that the method of literature-dependence does not over-
estimate linkages to such extent as to exhaust the
possibility of counting all potential links.
Supplementing GCA
Information about the presence or absence of potential
links between species may serve as fundamental infor-
mation for constructing food webs, provided that (a)
the study concerns itself only with web structure, not
with the frequency or strength of interactions (Polis
1991), and (b) a similar assemblage of the same preda-
tor and prey species have been studied previously.
When a new species is identified in an ecosystem, or
when the food habits of a known species are unknown,
GCA seems to be necessary for establishing linkages
with the other (onto)species in the system. However,
1000
L 500
10 20 30 40 50
5 food links as possible is the primary prerequisite. This
Fig. 1. The relationship of linkages with system size (S) for
II 500 randomized analogs of pond webs, created on rules of
non-random linkages inferred from published data. Each dot
is co-incident for at least 20 data points. The curves depict
power function relationships: (a) L=0.12S21O, and (b)
Lmax= 0.17S2.19
OIKOS 78:1 (1997)
estimation of links through GCA would be too arduous
and lengthy for large food webs. GCA for the rarer
species would 'be especially time consuming. Literature
dependence is perhaps the best option for the majority
of the rarer taxa whose food links are known (Carney
1995). For new linkage studies, Paine (1988) has ac-
knowledged the various means of estimating food links,
other than GCA: direct observation of the predation
act, scatology, indirect evidences, immunological study,
and "even plausible guesses". All these may supplement
published linkage data and even serve as a substitute
for fresh GCA, especially when GCA cannot be carried
out.
Performing GCA for a majority of species in the
immensely speciose tropical food webs, most of which
exist in the Third WorId, seems impossible to carry out;
apart from the unwieldy number of species, the paucity
of skilled researchers and/or the rarity and "endan-
gered" status of certain species that should not be
sacrificed for GCA, and/or the lack of infrastructure
and funds for food web research are the major impedi-
ments. In such cases, direct observations of predation
act and indirect evidences will be useful (e.g. Lieberman
and Lieberman 1987, Dinnerstein and Wemmer 1988).
Havens et al. (1996) have used a mixture of direct
measurements including bird nestling regurgitant sam-
pling, and inferences from published data.
Indigenous peoples in the Third WorId seem to have
a wealth of empirical knowledge about the food habits
of a large number of species. One effective way of
learning about the tropical systems in the Third WorId
countries would be to verify the indigenous people's
experiences about the food habits of different species
and their life history. Of course, one must be cautious
in recording such anecdotes, because many of them are
arrant superstitions (for example, a popular belief in
India is that snakes ingest banana and milk). On the
other hand, numerous items of folk knowledge, though
easily verifiable, are not even investigated, because they
are presumed by many to be scientifically unusable at
the best, and grossly unscientific at the worst. In the
light of post-modernist critique, this may be explained
as a legacy of the Western prejudices against indigenous
knowledge base in general. Thus, such facts as the
white-breasted kingfisher preying on rats, and the
greater adjutant stork consuming crow and domestic
chicken are hardly reported in scientific literature.
The question as to whether a particular linkage is too
infrequent to deserve estimation in food web statistics
seems secondary to the problem of high quality food
web description, for which identification of as many
could be facilitated by involving an army of local
indigenous people trained as "para taxonomists" (NRC
1992) for inventorying local biodiversity as well as for
food linkages. The folk knowledge, filtered through
trained observation, is likely to supply sufficiently de-
193
tailed information for high-resolution food web analy-
ses in the future.
Acknowledgements - This paper arose from an unknown
referee's comment on my previous Gikos paper that literature-
dependence might overestimate linkage estimation. I am grate-
ful to R. L. Brahmachary, P. Bhattacharya and S. R. Banerjee
for sharing valuable data, and to Heath Carney for perceptive
comments on the paper. I also thank Karl Havens and Heath
Carney for giving me the opportunity to read their unpub-
lished manuscripts.
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