Honeyguides and Honey Gatherers: Interspecific Communication in a Symbiotic
H. A. Isack; H.-U. Reyer
Science, New Series, Vol. 243, No. 4896. (Mar. 10, 1989), pp. 1343-1346.
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Fri Mar 14 02:33:43 2008
that results in an increase in the oscillator
strength of these excitations, such as we
have observed, could then turn on the super-
conducting phase transition. Even if the
mechanism is primarily phonon-mcdiated,
an anharmonic mode such as that described
here could have a much reduced isotope
etfect on T,than that expected from stan-
dard Bardeen-Cooper-Schrieffer phenom-
enology (29), as is found for YBa2Cu307
(35).This same mechanism could be opera-
tive in the other cuprate-based, axial oxygen-
containing superconductors, and especially
in the thallium- and bismuth-based com-
pounds, where these oxygen atoms are also
the bridge between the Cu02 planes and a
highly polarizable layer.
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(University of Washington, Seattle, August 1988);
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4. S. D. Conradson et al., in preparation.
5. S. M. Heald, J. M. Tratlquada, A. K. Mooden-
baugh, Y. Xu, Phys. Rev. H 38, 761 (1988).
6. N. Kosugi, H. Kondoh, H. Tajima, H. Kuroda,
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\ - ?
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103, 101 (1986).
12. As shown in (8) and (9),each particular transition to
a localized state in copper K-edge XANES can shift
by up to 3 to 4 eV as the coordination envinmment
is altered. Assune that a mimx phase is present at a
concentration of 5%, which is already much larger
than can occur in this san~ple. Then, because the
XANES are normalized on a per atom basis, and
using 0 5 as the absorbance of an individual tratlsi-
tion, the 1% changes in the absorbance we observe
represent 60% changes in the absorbance for the
trace phase. We cannot envisio~l any mechanism
whereby this change in oscillator strength would not
be accompanied by a large energy shift, especially for
four separate transitions. The energy should actually
be a better indicator of these kinds of changes than
the intensity, but the limitations of the experiment
are such that an absorbatlce difference of 1% or less
cat1 be measnred whereas at1 energy shift of 0.2 eV is
required to accompl~sh a11 observable change in the
difference spectrum. At a realistic minor phase con-
centration of 1%, the changes in the absorbance of
this phase would be 100% or greater, impossibly
13. ?S. D. Consadson, I. D. Raistrick, G. H. Kwei, in
14. J. J. Caponi et dl., Grvophys. L.nt. 3, 1301 (1987).
15. M. A. Beno et nl., Appl. Phys. Lrtt. 51, 57 (1987);
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10 MARCH 1989
Siegrist e f al., Phys. Rev. H 35, 7137 (1987); A.
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16. For the sake of a,nsistency, we have adopted the
same labels fix the final states as in (5) and (6).
Altl~ough we concur with the assignment of feature
C to thc Cul 4p,v +1s transition, to a final state
nlolecular orbital of v synimetry con~posed of the
Cul 411~ and 0 1 and 0 4 (3)p, atomic orbitals, we
believe that feature D, assigned to the Cu2
4p,v +1s transition, actu.lUy i~lvolved a find state
molecular orbital which is not strictly of v syrnmetry
because it possesses at least some 0 4 (3)p, character,
analogous to the Cu2 3d,2-04 2p, band near the
Fermi level. Another issue in these assignments is
the choice of the single- or multi-electmn model. In
the multi-electron model (10, ll), used in the assign-
ments for YBa2Cu307 (5, &), the find state of the
CID transition is the bou~ld Cu 4pv, and the lower
energy A ! B transition is assigned to the Cu
4pv + shakedown state. In the single-electron mod-
el (X), the final state of the CID transition is the
quasi-bound Cu 4pvL (L = ligatld), which differs
from the lower energy AIR transaion to the bound
Cu 4pv final state in that it is n~ore dek,calized, with
appreciable photoelectron density on ligatld-cen-
tered orbitals. If the single-electron model is correct,
because changes in the i~ltellsities of transitions are
more significant than changes in their energies, the
overlap is apparently affected more that1 the nature
of the 4pvL state. Therefore, our interpretation is
based only on the fact that the find states of these
transitions have Cul 4p, and Cu2 4p, character,
which has been observed experimentally (5, 6), and
is illdepcude~lt of the exact nature of the final state.
17. R. J. Cam et al., Physica R 153-155, 560 (1988).
18. M. Mali et al., Phys Lrff A 124, 112 (1987).
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(1987); J. B. Royce, F. Bridges, T. Claeson, K. S.
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(1987); E. D. Crozier, N. Alberding, K. K. Bauch-
spiess, A. J. Seary, S. Gygax, Phys. Rev. R 36, 8288
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Phys. Lett. A 122, 198 (1987); J. Yu, S. MassicIda,
A. J. Freeman, D. D. Koelli~lg, ibtd., p. 203.
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con. 1, 111 (1988).
22. T. Laegreid, K. Fossheim, F. Fassenden, Physica C
153-155, 1096 (1988); V. Mueller et al., ibid., p.
280; G. Canelh et al., ibid., p. 298.
23. ?U. Murek, J. Rolder, K. Keulerz, ibid., p. 270, S.
Della Longa et dl., paper presented at 5th Interna-
tional C:onference on X-Ray Absorption Fine Struc-
ture (University of Washington, Seattle, August
24. K. A. Butera, Phys. Rev. H 37, 5909 (1988); M.
Ishikawa ef al., Solid State Co~nnznn. 66, 201 (1988).
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al., E~~vophys. Lm. 4, 1145 (1987); M. Francois et
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M. Temmerman, Phys. Rev. R 37, 5158 (1988).
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on X-Rap Absorption Fine Stn~c-
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29. N. M. Plakida et al., E~~rophys.
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35. E. Garcia rt al., Phys. Rev. H 38, 2900 (1988).
36. We tl~ank C. Ponader, G. Kwei, M. Zietlow, S.
Ekberg, and the Stanford Sp~lchrotron Radiation
Laboratory (SSRL) operations staff for their assis-
tance in acquiring these data, J. D. Thompson for
the magnetic susceptibility measurements, and R.
Albers, K. Martin, J. Wilkins, A. Bishop, Z. Fisk,
and D. Smith for useful discussions and for review-
ing this manuscript, as well as K. Scott for the
XAFPAK data analysis software. Data acquisition
and some atldysis were done at SSRL, which is
fi~nded by the U.S. Department of Energy under
contract DE-AC03-82ER-13000, Office of Basic
Energy Sciences, Division of Chemical Sciences atld
the NIH Biotechnology Kesource Program, Divi-
sion of Kesearch Resources. This work was support-
ed by the Department of Energy via the Institutio~lal
Supporting Research Program and the Center fix
Materids Science at Los Alamos National Labora-
22 Novcmber 1988; accepted 24 Jatluar)~ 1989
Lett. 4, 1309 (1987).
Honeyguides and Honey Gatherers: Interspecific
Communication in a Symbiotic Relationship
In Inany parts of Africa, people searching for honey are led to bees' nests by the greater
honeyguide (Indicator indicator Sparrman). The Boran people of Kenya claim that they
can deduce the direction and the distance to the nest as well as their own arrival at the
nest from the bird's flight pattern, perching height, and calls. Analyses of the behavior
of guiding birds confirmed these claims.
honey in Africa for 20,000 years (1,2).Even
today, honey contributes significantly to the
diets of many African people (2-5). Whcn
searching for honey, Africans are often
joined by the greater honeyguide (Indic.atov
leads them to bee colollies
(Apis m?l/ififa)located in large trees, rock
crevices, or termite mounds. After the gath-
erers have opened alld left he
feeds 011 pieces of honeycomb left behind.
CCORDING TO ROCK PAINTINGS
from the central Sahara, Zimbabwe,
and South Africa, man has collected
From these it extracts mainly the larvae and
the wax to supplement its normal diet of
insects (5-7). The earliest written accounts
of this bird-man interaction date back to the
17th century (6). Because of the anecdotal
nature of most of these reports, however,
H. A. Isack, Department of Ornithology, Nationd Mu-
se~" of Kenya. Post Office Box 40658, Nairobi, Kenya.
13.-U. Kever. Max-Planck-Institut fiir Verhaltens~hvsio-
logic, D-8131 Seewiesen, Federal Kepubl~c of G&n;anp.
*Present address and address for reprint requests: Zoolo-
gisches Institut der Universitat Ziirich, Winterthurer-
strasse 190, cH-8057 Ziirich, Sw~tzerlatld.
flown) from the start of the tour to the
present pcrch (see Fig. 3A for an illustrative
We found all three Roran statements to bc
true. The closer the nest, thc shorter the
duration of thc first disappearance (Fig.
3A). When disappcaring, the bird probably
flies toward the nest to confirm its position
beforc starting a guiding tour. ~liether it
covcrs the wholc distancc or only flies until
it finds a conspicuous landmark, we cannot
Also, the closcr we approachcd the ncst,
the shorter the distancc bcnvecn stops, cspe-
cially during the last 200 m (Fig. 3B)
(P = 0.011, Wilcoxon test; 11). Stopdist
was not significantly rclated, howevcr, to
DistAown and Stopno (both P > 0.180).
Thus, first disappcarancc and stopping dis-
tance reflcct the rcrnaining distance to the
nest. Conversely, perching height reflects
the number of stops and the distance alrcady
covcred since the tour startcd. Perch de-
creased with Stopno (Fig. 3C) and Dist-
flown (not shown in Fig. 3;
-0.002 2 0.001, P = 0.015) (12). As guid-
ing is fairly dircct (Fig. 2, B through E), an
increase in Stopno and Disdlown norrnally
leads to a decrease in Nestdist. Thus, our
results confirm the honey gatherers' obser-
vation that the bird perches lowcr as it gets
closcr to the colony. The rcsults do not,
however, confirm their intcrpretation that
perching height indicates the distance to the
ncst; Perch was not significantly related to
Nestdist (P - 0.275).
Arrival. Boran honey gatherers nlaintain
that they can tell from changes in the bird's
behavior when it has reached its goal. We
found two behavioral changcs to support
this statement; one is rclated to the call, the
other to the flight pattern. On arrival at the
ncst, the bird perches close to it and emits
the "indication call" (Fig. 1B). This call
differs from the prcvious guiding call in that
it has a softer tone, with longcr intervals
between successive notcs. There is also a
diminished responsc, if any at all, to whis-
tling and shouting by humans. After a few
indication calls, thc bird remains silent.
Whcn approachcd by the searching gather-
er, it flies to another pcrch close by, somc-
times after circling around the nest. The
resulting flight path (Fig. 2R) finally reveals
the location of the colony to the gatherer. If
thc honey collector does not (or prctends
not to) dctect the nest, the bird gives up
after a while. It may thcn leave thc area
either silcntly or start a guiding session to
anothcr colony. In the latter case, it switches
from the indication call to thc gliding call
and resumes a fairly dircct flight pattern.
Although a fi:w investigators (7) have
assumed that greater honeyguides know thc
location of one or more bcc colonies in a
particular area, thc prevailing opinion still is
that the bird docs not know wlicrc. it is
taking a person but rather "lcads in a most
erratic course" until the sight and sound of
incidentally encountered bees brings thc
guiding to a halt (6, 13). The very first
discovery of a colony may indeed depend on
such signs; but thercaftcr the birds (regular-
ly?) monitor the nests even when no guiding
is taking placc. From camouflaged obscrv-
ing positions occupied befi~rc dawn, we
observed several marked and unmarkcd hon-
eyguides visiting a nest. They always ap-
pearcd singly, stayed for only about a min-
ute, and thcn flew away. When the bccs
wcre still docilc, as on cloudy and cool
mornings, the bird would fly straight into
thc entrance of the nest and pcer into it.
The information gathcred during such
visits cnables the bird to engage in its gonl-
oricnted guiding behavior. Our finding that
native people are able to interpret this pnt-
tern reliably is, howevcr, not equivalent to
saying that every aspect of the bird's guiding
bchavior is meant to inform them. The
changcs in call and flight pattern aftcr the
arrival (Figs. 1 and 2B) probably are infor-
mativc; but thcre are more parsimonious
explanations for other aspects of the bird's
bchavior. Thc directional flight (Fig. 2A)
and the duration of the first disappearance
(Fig. 3A) are inevitable results of a bird
flying to a nest that it knows. Thc reduction
in perching hcight (Fig. 3C) could be due to
tlic honeyguide's gradual loss of fcar of the
fi,llower. Similar cases of distances dccrcas-
ing over time are known from mobbing
birds arid other animals interacting with
predators ( 14, 15). Decreasing risk and fcar,
howcvcr, are unlikely to account for the
reduced distance bctwcen stops (Fig. 3B),
bccausc Stopdist decreased neither with Dist-
flown nor with thc frequency with which the
bird had been approachcd (Stopno). Also, the
bird allows people to approach to within 5 to
15 m of its perch, much closer than even the
shortest average stopping clistance of 20 m
We suggest that thc dccrcasing Stopdist
represents an "area-restrictcd scarch" (16)
that is pcrformcd by many animals when
close to their goal, be it food, hosts, or
homes ( 1 7-19). One conlmon characteristic
of this scarch pattern is reduccd step length
and thus speed. Conseclucntly, the animal
spends morc time scanning the promising
area and is morc likely to detect signs of the
goal, such as swarming becs or specific
landmarks. This will enable it to correct
directional crrors (compare thc smaller di-
rectional variance toward thc end) to avoid
an overshooting or even missing (dotted
linc in Fig. 2R). Farther away from the nest,
longer stopping distances may bc more cco-
noniical because they reduce the numbcr of
cncrgetically expensive maneuvers associat-
ed with takeoff' and landing. According to
this interpretation, distances bctween thc
final stops should dccreasc when any feature
impcdes detection of tlic nest (for cxample,
dense vegetation). Unhrtunately, our prc-
sent data do not allow us to test this predic-
tion, but the high variation in stopping
distances may have resulted partly from such
diff'ercnccs in visibility. This high variation
also makcs it unlikely that the bird "deliber-
ately" tclls the follo~ver wherc to look pre-
cisely for thc nest.
Our data also do not yet allow us to tcst
thc following two claims of Boran honey
gathcrers: (i) that a bird, flying lower than
the tree tops, will guide to a colony closc to
the ground, and (ii) that when nest distances
become very long (about 2 km or more), the
birds "dcceive" the gatherers about the rcal
distancc by stopping at shorter intcrvals.
Howcver, having found all the other Boran
5 ; 0-
1200 800 LOO
Distance to nest (m)
E 80J B
.- $ L O
loo --7 o +f\
Distance to nest (m)
Stops since encounter
Fig. 3. (A) 1)uration of first disappearance, (B)
stopping distance, and (C) perching height in
relation to ncst distancc (A and B) and number of
the stop (C), respectively. Shown in (B) are the
means and standard deviations calculated from
pooling data within the same 50-m category of
ncst distance (1 to 50, 51 to 100, . . ., 451 to 500
m). (A) and (C) give the original data together
with the respective regression lines. Their slopes
(b +- SE) are 0.059 a 0.019, P = 0.007 [(A),
linear model] and -0.115 +- 0.034, P = 0.002
[(C), exponential model].
observations to be true, we see no reason to
doubt the statements of these excellent
REFERENCES AND NOTES
E. Whittal, Rokmakierie 20, 73 (1968). ?
EI. Pager, Ree World 54, 61 (1973). ?
G.W. B. Huntingford, Anthropoi 50, 602 (1955).
4. M. Icliikau~a, A-j. Study Monqyr. 1, 55 (1981).
5. 11. A. Isack, thesis, ?Oxford University, Oxford
6. 11. Friedi~aui. Uuli U.S. Natl 12,flls. 208. 111955).
7. I<. L. Short and J. F. M. Ilorn, A m . us.,
2825, 1 (1985).
8. E. Bartsclielet, in ?At~itizal Mijiratiot~, Navijiatiotr and
hot win,^, K. Schmidt-Kocnig and W. 1 ' . Kccton,
Eds. ('~~ringcr-verlag, Rcrli;,
9. l'hc obscrvatioll that stopping distances dccrcase as
the bees' nest IS approached was also reported by G.
W. Stow [The Native Races oJ South Ajica (Swat1
Sonnenschcin, London, 1905)].
10. We mcasured distances by countillg paces and later
converting them into meters. l'crching heights were
estimated to the nearcst 0.5 m. In cases of skewed
1978), p. 3.
distribution, original data were log-transformed.
11. l'hc ? relatioll betwccll Stopdist and Stopno was
tested wlth111 guidings, yielding one regression coef-
ficient (h) for each tour. The relations between
Stopdist and Ncstdist and Distflown, rcspcctivcly,
were tested across gui&ings. In the case of Ncstd~st,
separatc rcgressiolls were calculated for each
Stopno, whereas, in the case of Dlstflown, separatc
regressions were calculated for each 50-m category
of Nestdist. In all cases, the regression cocfficients
werc then tested against the 0 hypothesis of no
relation (b = 0) by mcms of a Wilcoxon matchcd-
pairs, signed-ranks test.
12. Thc small sample size did llot allow us to calculate
separatc rcgrcssions as in the case of Stopdist.
'Shcrefore, Pcrch data from all guidings were
13. Our reanalysis of Friedmann's data (6) indicates that
cvcn his birds showed directional guiding and prob-
ably had prior knowledge of the hive location (13. A.
Isack and I<.-U. Rever. in nrcuaration\.
14. E. Curio, G. ~ l u m i , K. licgelmalul, <jecoloRia (Uer-
!IN)60, 83 (1983).
15. M. Milinski, Narlrre 325, 433 (1987).
16. J. R. Krcbs, in Behaviolrral Ec~lo~yy-An Evollrtionar)'
Approach. J. R. Krcbs and N. B. Davics, Eds.
Structure of Recombinant Human Renin, a Target for
Cardiovascular-Active Drugs, at 2.5 A Resolution
The x-ray crystal structure of recombinant human renin has been determined.
Molecular dynamics techniques that included crystallographic data as a restraint were
used to improve an initial model based on porcine pepsinogen. The present agreement
factor for data from 8.0 to 2.5 angstroms (A) is 0.236. Some of the surface loops are
poorly determined, and these disordered regions border a 30 A wide solvent channel.
Comparison of renin with other aspartyl proteinases shows that, although the
structural cores and active sites are highly conserved, surface residues, some of which
are critical for specificity, vary greatly (up to 10 a). Knowledge of the actual structure,
as opposed to the use of models based on related enzymes, should facilitate the design
of renin inhibitors.
(Klackwell, Oxford, 1978 ), p. 23.
17. M. P. EIassel alld li. M. May, J.At~itiz. Ecol. 43, 567
18. J. N. M. Smith, Uehaviour49, 1 (1964).
19. R. Wehner and M. V. Srin~vasan, J. Comp. Physiol.
142, 315 (1981).
20. ?We thank thosc who supported the study, in partic-
ular R. E. Lcakey, C. M. l'errins, 1. Orto, S. Orto,
and thc honey collectors G. Dambi, D. Galgallo, and
A. Mariiqo. Financial and logistic support was pro-
vided by thc African Wildhfe Foundation (Nairobi),
East Afr~can Wildlife Society (Narobi), Frank
Chapman Memorial Fund (New York), M u -
l'lanck-Institut fir Verhaltensphpsiologie (Seewie-
sen, FliG), National Museum of Kenya (Nairobi),
Percy Sladen Memorial Fund (I<ondon), and thc
Christopher Welch Scholarship (Oxford). H. G.
Wallraff and A. D. Rarbour helped with the statis-
tics. R. Diesel, J. Lamprecht, F. Trillmicli, W.
Wicklcr, and two anonymous referees made useful
comments on an earlier draft of the paper. G. Louw
improved the Enghsli. This report is dedicated to
the late H. Fr~edmann, the ploneer of honcyguidc
21 Juue 1988; accepted 14 December 1988
to 6% polyethylene glycol 600 buffered with
50 ml/lNaH2P04-I<2HP04 to pH 4.7. The
resulting crystals exhibited tetragonal sym-
metry, space group 14,wit11 unit-cell dimen-
sions, a = b = 133.5 A, c = 41.7 A, wit11
one renil1 molecule per asymmetric unit,
VM = 2.53 A3 per dalton.
Intensity datd were collected on a twin
multiwirc detector system (12). A total of
60,5 12 measurements (13,343unique data)
were measured from a single rcnin crystal.
The overall symmetry agreement factor
[= C(li- (I))/Z(l),where 1are the net intcn-
sities] was 0.09.The structure was solved by
the molecular replacement method (13).
Several renin models bascd on the ltnown
structures of three fungal aspartic protein-
ases have been built (14). The more exten-
sive homology among marrlnlalian species
led us to construct a search model for renin
bascd on the molecular structure of porcine
pcpsinogen (15, 16). Thc correlation coefi-
cient between observed and calculated struc-
ENIN (E.C.126.96.36.199)IS A HIGHI;Y
specific aspartyl protcinasc with
.only one known substrate, angio-
tensinogcn. In humans, a decapeptide, angi-
otensin I, is released from angiotensinogcn
by the catalytic hydrolysis of the 1,eu"'-
Val" bond. Angiotensin I is processed by the
angiotensin 11, a potent vasoconstrictor in-
volved in regulating blood pressure and
fluid balance. However, presently available
therapeutic agents for reciucing blood prcs-
sure target ACE (1) and not rcnin.
Because only very s~nall quantities of kid-
ney renin have been available, much of tl~c
biochemical characterization of renin has
been done on the rnouse submaxillary gland
enzyme. Mouse renin has been protein- (2)
and c1)NA-sequenced (.?), anci crystals of it
have been reported by sevcral groups (4, 5).
In the five crystal forrns of mouse rcnin
enzyme (ACE) to
obtained, the corresponding asymmetric
units contain multiple copies of the mole-
cules (i), which complicates the crystallo-
graphic problem enormously. No f~~rthcrture factors based on the oriented and trans-
progress in this analysis has been rcported.
The primary structure of the human cn-
zynle has been deduced solely from cL)NA
(6) and gene sequences (7). We converted
secreted hurnan prorenin (8) from transfect-
ed Chinese hamster ovary cells (8, 9) to
active renin by cleavage with immobilized
trypsin. The purified recombinant hu~nan
(rh) renin (10) was treated with endoglpco-
sidase F to remove attached carbollydrates
without affecting the specific acti\lity of the
final product (I I).
Sample l~omogeneity from batch to batch
was difficult to regulate. Most preparations
exhibited three to five bands on isoclectric
focusing gels. Prom -1500 diCerent ci-ytal-
lization trials, the optimal conditions werc 5
lated nod el was 0.39 (9.5a above the mean)
for the data in the 6 to 4 A resolution shell.
The corresponding K factor 1 = 81/1:,/ - ll:,ll/
CjFo/, where /Pol and /I:,/ are observed
and calc~ilated stmcnlrc factor amplinidcs]
A. R. Siclcck~,K.I I.ly.lk.~wa, M. Fullnag&,M. E. P.
Murphv, M. Fi-.~sei-,A. I<. Muir, i M . N. G. Jamc,
M C ~ I C ~
Rcscarch (:ounc~l of (:anada
Stmcturc .~nd Function, llcpartment of Riocheniistry,
Uni\.crsltv <~iAlbert.l. Edmonton. Alberta. C.~n.tda 'I'6G
C. 'I'.(:arilli and J. A. Lewiclii, <:aliforn~.~
Tric., klountain View, CA 94043.
J. 1). Rater, Metabolic Rese.~rch Unit, Unkersin of
(:.~liforn~.~, S.ln Fr.lncisco, <:A 94143.
Group In Proteln
*Present address: L.~horatotv of Phvalcal <:hcmiatr\.,
Cnlvcrsln of Gronlngc~l, N'~jenhorgh 16, 9747 Ai;,
Groningcn, 'l'lic Nctherlands.
S<:IENCE, VOI,. 243