COTURNISM: Poisoning by European Migratory Quail
Old World migratory quail (Coturnix) are classified by
territorial range into three subspecies. The European C. coturnix coturnix,
common to Europe, North Africa, and western Asia, has been reported toxic while
both Asian C. coturnix japonica and African C. coturnix africana subspecies have
not been, heretofore, identified as poisonous. This essay examines the antiquity
of coturnism or human food poisoning by migratory quail, its symptoms,
contemporary distribution, and possible etiologies, and concludes with
suggestions for research on this ancient, curious dietary problem.
EUROPEAN MIGRATORY QUAIL: DISTRIBUTION, HABITAT, AND MIGRATION
The European migratory quail (Fig. 1) is a Palaearctic species distributed from
Arctic Europe southward to equatorial Africa. It possesses a west—east range
from the Atlantic islands near Africa through Pakistan, northern India, and the
central Soviet Union (Bannerman, 1953; Mackworth-Praed and Grant, 1957;
Dement’ev et al., 1967; Etchecopar and Hue, 1967). Within this broad area quail
maintain habitat from sea level to above 2500 m, preferring agricultural fields,
grasslands, and other protective vegetation offering a diet of mixed seeds,
ground-dwelling insects, and small invertebrates (Voous, 1960; Reese and Reese,
1962).
FIGURE 1. European migratory quail (Cotumix cotumix
cotumix)
In preparation for migration quail gain nearly 50% body
weight. Such fat stores result in large, plump quail
that are sharply differentiated from representatives at
other times. Quail migration northward from equatorial
Africa begins in late winter and lasts through spring.
Quail breed in European grain fields from late spring
through summer, whereupon they return to sub-Saharan
Africa between August and October (Lynes, 1909; Moreau,
1951; Bannerman, 1953). While their migration pattern is
complicated and not well understood, quail generally
follow one of three major north—south flyways (Fig. 2).
The western flyway extends northward across West Africa,
the western Sahara, northwest Africa, and western Europe.
This route is characterized by a difficult trans-Saharan
crossing, but relatively easy passage over the narrow
western Mediterranean Sea. The central flyway includes a
difficult transSaharan and Mediterranean crossing.
Beginning in equatorial central Africa the central route
extends northward to western Libya and Tunisia,
ultimately reaching west coastal Italy and west-central
Europe. The eastern flyway begins in the Great Lake
region of East Africa and is characterized by a
relatively easy northward flight along the Nile River
basin to Egypt, where the flyway splits into eastern and
western components. The eastern branch crosses southwest
Asia (Israel, Lebanon, Syria, and Turkey) and terminates
in the western Soviet Union, while the western branch
crosses the Mediterranean at its broadest point and
extends across mainland and insular Greece, ultimately
reaching eastern Europe.
FIGURE 2. Geographic range and flyway patterns (Coturnix
cotumix cotumix)
MIGRATORY QUAIL AND HUMAN POISONING
Coturnism, or food poisoning by migratory quail, while
recent in name has been documented for at least 2500,
possibly 3500 years. The early date stems from a
Biblical account (Numbers, 11:31—34) when Israelite
consumption of migratory quail in Sinai during the
Exodus resulted in numerous deaths. Whatever the
validity of the Biblical account, coturnism certainly
was known to ancient Greek and Roman naturalists,
physicians, and theologians, among them Aristotle (On
Plants, 820:6—7), Didymus (Geoponics, 14:24), Lucretius
(On the Nature of Things, 4:639—640), Philo (The Special
Laws, 4:120—131), Galen (De Temperamentis, 3:4), and
Sextus Empiricus (Outlines of Pyrrhonism, 1:57).
Central to these Greek and Roman reports is the thesis
that migratory quail become toxic after consuming seed
from hemlock (Conium maculatum) or henbane (Hyoscyamus
niger). The ancient reports state that quail were not
affected adversely by the seed but could transmit plant
toxins to humans who dined on such birds. Indeed, the
Roman Pliny (NaturalHistory, 10:33) revealed that
migratory quail were banned as human food in Italy
during the 1st century A.D., presumably because of
potential toxicity.
Medical-toxicological interest in coturnism continued
into the Medieval period as evidenced by writings of
prominent Islamic and Jewish scientists, among them Ibn
Sina (The Canon, 2:2:2:5), Moses ben Maimon (Comment.
Epidemiarum, 6:5), Qazwiny (Kitab Aga’il, 2:250), and
al-Demiry (Hayat al-Hay- awan, 1:505). Such Islamic and
Jewish accounts focused on the relationships between
quail diet, the plants aconite (Aconitum napellus) and
hellebore (Veratrum spp.), and subsequent human
poisoning.
Nineteenth and twentieth century writers, among them
Cornevin (1887), Lewin (1898), and Grieve (1931),
suggested that quail are insensitive to hemlock. More
recent authors, however, have challenged the thesis that
coturnism is due to hemlock by suggesting that quail
become poisonous after consuming insects with elevated
levels of Aristolochic acid (Rotschild, 1970), or after
eating seeds from cyanogenic species (Tullis, 1977).
Work by Kennedy and the present author (Kennedy, 1980;
Kennedy and Grivetti, 1980; and Grivetti, 1980) has
contradicted the hemlock thesis by demonstrating that
quail are sensitive to hemlock alkaloids and die after
consuming only 0.1 g hemlock seed. Thus, the etiological
mechanism(s) for coturnism transmission to humans remain
unclear.
COTURNISM: DISTRIBUTION AND SYMPTOMOLOGY
Human poisoning by quail has been reported during the
twentieth century from Algeria, France, Greece, and
Russia; ancient accounts suggest coturnism in Italy and
the northern Sinai peninsula (Kennedy and Grivetti,
1980). Reports by scientists and physicians reveal
substantial variation in symptoms attributed to
coturnism. In Algeria reports include colic, diarrhea,
vomiting, fatigue, sensation of heaviness in the lower
extremities, impaired speech, and lower limb paralysis (Sergent,
1941). Across the Mediterranean in southern France
symptoms associated with quail poisoning include
respiratory distress and appearance of red, itchy
urticaria (Sergent, 1948). In Russia, in the region
between the Black and Caspian Seas, symptoms of
coturnism include general weakness in the legs occurring
3—4 hr after consumption, sharp pains extending from the
legs upward through the torso into the neck lasting 2—12
hr, followed by generalized pain and weakness continuing
for 3-10 days (Khovanskii, 1954, 1957, 1964).
Coturnism is described in detail from the Greek island
of Mytelene. There, symptoms have included anuresis,
myoglobinuria, sharp muscular pains along the trunk and
extremities graduating to paralysis in muscles recently
used, oliguric to anuric urinary output, azothemic blood,
elevated uric acid levels, elevated SGOT levels (Serum
Glutamic Oxaloacetic Transaminase), respiratory distress,
and death (Hadjigeorge, 1952; Ouzounellis, 1968a, 1968b,
1970). Demographic evaluation of coturnism cases from
Mytelene reveals a greater propensity for poisoning
among active, adult males than among females (Ouzounellis,
personal communication, 1970). Unpublished accounts
document coturnism on the Greek mainland, specifically
at Marathon northeast of Athens (Ouzounellis, personal
communication, 1970).
COTURNISM: CONTINUED SEARCH FOR THE TRANSMISSION
MECHANISM
It has been widely held from antiquity through the
twentieth century that poisoning from migratory quail is
due to quail diet, specifically an intake pattern based
on hemlock or another toxic alkaloid, perhaps aconite,
hellebore, or henbane. First scientific experiments into
the mechanism for transmission of coturnism to humans
were conducted by Sergent (1941). Quail used in his
experiments were healthy, evicerated, thoroughly cooked,
and free of pesticide residue (a twentieth century
precaution!). Sergent reported that quail in Algeria
consumed hemlock (Conium maculatum), hellebore (Hyoscyamus
niger), and black morelle (Solanum nigrum) and deduced
that the birds became toxic after consuming seeds of
these plants. He reportedly fed hemlock to quail but
could not produce symptoms typical of hemlock poisoning;
such dosed quail were fed to dogs and the canines
subsequently exhibited hind-leg paralysis, one of the
classical symptoms of hemlock poisoning. Sergent
concluded that quail were insensitive to hemlock and
that quail flesh would transmit hemlock toxins to
animals.
Experiments on migratory quail (Asian subspecies
available as an experimental animal) by Kennedy and
Grivetti (1980) could not reproduce Sergent’s findings
and demonstrated that hemlock ingested by quail at the
quantity of 1.3—0.1 g daily produced classical symptoms
of hemlock poisoning and death. Additional experiments
demonstrated that quail, if provided a choice, would not
select hemlock as food. Other experiments reported that
hemlock ingested by quail in quantities of less than 0.1
g daily would produce a significant appetite depressant
effect.
Among the questions to be resolved, therefore is, do
migratory quail consume hemlock under free-ranging
conditions? Despite ancient nineteenth and twentieth
century accounts suggesting hemlock as a regular
component of migratory quail diet, proof must lie in
botanical examination of seeds found in quail crops.
While numerous accounts suggest that quail consume, even
thrive on hemlock, this species has not been repeatedly
identified by botanists/ ornithologists as a component
of quail nutriture (see Cheesman and Sclater, 1935;
Uljanin, 1941; Witherby et al., 1949; Keve et al., 1953;
Heim de Balsac and Mayaud, 1962; Dement’ev et al., 1967;
von Blotzheim, 1973; and Bateman, 1977). The only
twentieth century account reporting hemlock in quail
crops is Sergent (1941) and a close reading of his text
suggests that the identification was made by hunters,
not botanists.
More significant, however, is the finding that ingestion
of hemlock by quail produces an appetite depressant
effect (Kennedy, 1980). Given the supposition that quail
might consume hemlock, to do so during the premigratory
stage when body weight must be nearly doubled would be
counter-productive. Since quail are toxic during the
migratory period and since the difficult transSaharan
and trans-Mediterranean flights necessitate increased
fat stores, one must logically exclude hemlock as the
mechanism for transmission of coturnism.
A further argument against hemlock is based on
seasonality and timing of the quail migration. In North
Africa quail migrate and reach Algeria primarily between
April and June, yet hemlock does not drop seeds until
late summer and fall. Consequently, before hemlock is
available for quail consumption the quail flocks have
already crossed the Mediterranean to Europe. When quail
return to Algeria from France during the fall, hemlock
seed is available yet the birds are not toxic at this
time.
Another major question for consideration is why are not
all quail toxic, or phrased a different way, why are
there not more reported cases of co- turnism? It is
apparent that coturnism is only recently receiving
epidemiological and medical attention in detail.
Ouzounellis is surely correct when he suggests that the
incidence of coturnism is underreported. But given
underreporting, other nagging questions remain. Why
should quail be toxic on the northward flight to Algeria,
but not the southern? Why are males more susceptible
than females to coturnism? Could such a pattern be due
to cultural traditions of serving quail primarily to men
as returning hunters, or could coturnism have a genetic
basis?
Given the wide range of symptoms identified with quail
poisoning, is coturnism a single or multiple disease? Do
different symptoms reflect differences in quail diet at
the local level? Does the absence or presence of
coturnism, after correlation with quail migration
direction, support a dietary basis for the disease, or
might flight stress in one direction and ease on the
return flight suggest production of a metabolite that
elicits coturnism in sensitive individuals or
populations?
Thus, it becomes important to clearly document each
instance of coturnism to permit evaluation of both
dietary and metabolite hypotheses. If quail diet is
central to understanding coturnism, logic holds that the
dietary elements investigated be lipophyllic, produce no
effect on quail, but cause poisoning in humans. In this
light, the report by Rotschild (1970) that migratory
quail are insensitive to aristolochic acid—a compound
common to certain insects on which quail dine—should
receive experimental attention. If quail physiology and
migration stress underlies coturnism, one would expect
outbreaks along the flyway stress localities, especially
among hunters who capture birds, dispatch them quickly,
and consume them within a few hours.
In addition to clearly documenting instances of
coturnism, data should be gathered on patient demography,
exercise activities prior to onset of symptoms, time and
seasonality of the attack, and cultural information on
methods used to obtain quail. Penning or cooping wild
birds would permit physiological recovery and excretion
of potentially toxic metabolites. Finally, data should
be collected on cooking and preservation techniques to
clearly differentiate between coturnism in the strict
sense and poisoning resulting from unsanitary food
preparation.
SUMMARY
Coturnism is ancient, traceable certainly to the Greeks
and Romans, possibly earlier. Human poisoning by quail
has been reported during the twentieth century from
Algeria, France, Greece, and Russia; ancient accounts
suggest coturnism in Italy and northern Sinai. Multiple
symptoms exhibited locally by humans consuming toxic
quail suggest that coturnism may have multiple origins
founded in local quail diet or in the production of a
metabolite during stress of migration. Such hypotheses,
however, remain unconfirmed and the mechanism of
transmission to humans remains unclear.
Present knowledge of coturnism, its distribution and its
history, permits an additional conclusion to be drawn.
Based on contemporary data of quail migration direction,
flyway patterns, and seasonality of flight, the Biblical
account of quail poisoning in Sinai may reflect an
actual event. If so, Israelites of the Exodus would have
been poisoned by quail during the months of
August-October and the Israelite encampment mentioned in
Numbers (11:31—34) would have been adjacent to the
Mediterranean coast. The disease now called coturnism
thus provides support for Biblical scholars who have
argued against tradition for a northern Exodus route in
contrast with the more widely held southern, tortuous
passage.
Louis E. Grivetti, Department of Nutrition,
University of California, Davis, California, USA
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