Content uploaded by Cristiano Dal Sasso
Author content
All content in this area was uploaded by Cristiano Dal Sasso
Content may be subject to copyright.
Nature © Macmillan Publishers Ltd 1998
8
letters to nature
NATURE
|
VOL 392
|
26 MARCH 1998 383
parasitized by other females. At the population level, parasitic eggs
decrease the average value of the parental eggs laid by parasites, in
turn favouring even greater allocation to parasitism (trade-off in
Fig. 1): optimal clutch size depends on the frequency of parasitism,
and vice versa. The dynamic nature of the problem is further
enhanced in species where the success of parasitic eggs is also
frequency-dependent22. These various game aspects do not alter
the qualitative assumptions or predictions of the graphical model. It
will be important, however, to incorporate these assumptions and
predictions into a more quantitative, theoretical study and into
some empirical tests. For example, in populations in which parasites
are also hosts, the fitness estimates for a parasite’s own clutch must
reflect her risks and costs of being parasitized. I have accounted for
these fitness estimates; egg survival estimates (Fig. 2) included
parasitic females who were themselves parasitized (6 of the 23
parasitic females). Some of these females raised parasitic chicks
and, consequently, sacrificed some of their own chicks in the
process.
Here I have shown that, for some species, clutch size cannot be
understood without considering conspecific brood parasitism. The
opposite is also true, and this clutch-size model provides a new
framework for understanding brood parasitism. Most studies of
parasitism do not examine clutch-size constraints and cannot
explain why parasites lay eggs in the nests of others rather than in
their own nests; in some cases, the hypothesis that parasitism yields
a direct increase in mean fitness has been prematurely rejected23.
Earlier studies of brood parasitism now need to be reassessed. By
integrating two fields of research that are generally considered in
isolation of each other—study of clutch size and conspecific brood
parasitism— this new clutch-size model provides a framework for
enriching our understanding of both fields. M
.........................................................................................................................
Methods
Comparing survival of parental and parasitic eggs. Brood parasites were
identified using standard techniques12. Eggs were considered successful
(fledged) if the chicks survived to 30 d after hatching12. As it is the fitness of
parental eggs relative to the fitness of parasitic eggs that is important, survival to
independence is a good measure of relative fitness, assuming that post-fledging
mortality is similar for both egg types. Survival rates for eggs in parasitic
females’ own nests were calculated for successful nests (some eggs hatched) but
then adjusted by the proportion of parental eggs that were laid in successful
nests (82.1% of 731 eggs). Only nests where the fates of more than half the
chicks were known were included in these analyses. Confidence limits for
proportion of eggs surviving (Fig. 2) were based on sample size24 for observed
eggs and on 1,000 bootstrapped regression equations for predicted next eggs.
For statistical comparisons of egg survival, a G-test compared last parental eggs
with parasitic eggs, whereas 1,000 bootstrapped predictions of ‘next’-egg
survival were used to compare ‘next’ eggs with parasitic eggs.
I examined egg success in relation to an egg’s position in the laying sequence
(backwards from the last egg laid in the clutch), rather than on the basis of
clutch size, to enable pooling of results despite large variations in clutch size12
and to predict what parasites would gain if they were to add ‘hypothetical’ next
eggs in the laying sequence to their clutches (Fig. 2). The survival value of eggs
from a specific position in the laying sequence would not indicate the fitness
increments from those eggs if later-laid eggs survive at the expense of earlier-
laid eggs, because the survival of the eggs would need to be discounted by the
fitness reduction they caused through the death of siblings. However, the two
measures (survival and fitness increment) will be equivalent where there is
strict laying-order-dependent survival within broods; in this study, few later-
laid eggs survived at the expense of earlier-laid ones12,16.
Clutch- and brood-size comparisons. For analysis of sizes of clutches of
parasitic and non-parasitic females, host availability was determined on the
basis of the observed spatial and temporal patterns of host use15. To reduce
variance due to strong seasonal decline in clutch size, the effects of date were
controlled by analysis of covariance (ANCOVA) (F¼9:04, P¼0:002); clutch
sizes (Fig. 3) are therefore adjusted means. For chicks, the assumptions of
ANCOVA are violated, so analysis of variance was used (F¼0:64, P¼0:53)
but, to avoid bias due to differences among groups in timing of nesting, only
birds who initiated laying within 20 d of the first egg laid in the population are
included.
To avoid potential confounding effects of female quality in the analysis of
host clutch-size responses, only host nests were included in these analyses.
Residual clutch sizes from regressions of clutch size against laying data were
used to control for strong seasonal declines in clutch size21.
Received 30 May; accepted 11 December 1997.
1. Lack, D. The significance of clutch size. Ibis 89, 309– 352 (1947); Ibis 90, 25–45 (1948).
2. Klomp, H. The determination of clutch size in birds, a review. Ardea 58, 1– 124 (1970).
3. Martin, T. E. Food as a limit on breeding birds:a life histor y perspective. Annu.Rev. Ecol. Syst. 18, 453 –
487 (1987).
4. Godfray, H. C. J., Partridge, L. & Harvey, P. H. Clutch size. Annu. Rev. Ecol. 22, 409– 429 (1991).
5. Yom-Tov, Y. Intraspecific nest parasitism in birds. Biol. Rev. 55, 93–108 (1980).
6. Andersson, M. in Producers and Scroungers (ed. Barnard, C. J.) 195– 228 (Croon Helm, London,
1984).
7. Rohwer, F. C. & Freeman, S. The distribution of conspecific nest parasitism in birds. Can. J. Zool. 67,
239–253 (1989).
8. Brown, C. R. Laying eggs in a neighbor’s nest: benefit and cost of colonial nesting in swallows. Science
224, 518–519 (1984).
9. Gibbons, D. W. Brood parasitism and cooperative nesting in the moorhen, Gallinula chloropus.Behav.
Ecol. Sociobiol. 19, 221–232 (1986).
10. Møller, A. P. Intraspecific nest parasitism and anti-parasite behaviour in swallows Hirundo rustica.
Anim. Behav. 35, 247–254 (1987).
11. Emlen, S. T. & Wrege,P. H. Forced copulation and intra-specific parasitism: two costs of social living
in the white-fronted bee-eater. Ethology 71, 2–29 (1986).
12. Lyon, B. E. Brood parasitism as a flexible female reproductive tactic in American coots. Anim. Behav.
46, 911–928 (1993).
13. Jackson, W. M. Causes of conspecific nest parasitism in the northern masked weaver. Behav. Ecol.
Sociobiol. 32, 119–126 (1993).
14. Maynard Smith, J. M. Evolution and the Theory of Games (Cambridge Univ. Press, 1982).
15. Lyon, B. E. Tactics of parasitic American coots: host choice and the pattern of egg dispersion among
host nests. Behav. Ecol. Sociobiol. 33, 87–100 (1993).
16. Lyon, B. E., Eadie, J. M. & Hamilton, L. D. Parental preference selects for ornamental plumage in
American coot chicks. Nature 371, 240–243 (1994).
17. Andersson, M. & Eriksson, M. O. G. Nest parasitism in goldeneyes Bucephala clangula: some
evolutionary aspects. Am. Nat . 120, 1–16 (1982).
18. Power, H. W. et al. The parasitism insurance hypothesis: why starlings leave space for parasitic eggs.
Condor 91, 753–765 (1989).
19. Eadie, J. M. Alternative Reproductive Tactics in a Precocial Bird: the Ecology and Evolution of Brood
Parasitism in Goldeneyes. Thesis, Univ. British Columbia (1989).
20. Rothstein, S. I. Brood parasitism and clutch-size determination in birds. Trends Ecol. Evol.5, 101 –102
(1990).
21. Lyon, B. E. The Ecology and Evolution of Conspecific Brood Parasitism in American Coots (Fulica
americana). Thesis, Princeton Univ. (1992).
22. Eadie, J. M. & Fryxell, J. M. Density-dependence, frequency-dependence, and alternative nesting
strategies in goldeneyes. Am. Nat. 140, 621 –641 (1992).
23. Brown, C. & Brown, M. B. A new form of reproductive parasitism in cliff swallows. Nature 331, 66 –68
(1988).
24. Sokal, R. R. & Rohlf, F. J. Biometry (W. H. Freeman, San Francisco, 1981).
Acknowledgements. I think P. Grant, D. Rubenstein, C. Martinez del Rio and H. Horn for advice during
the study; R. Cartar, J. Eadie, D. Hill, A Kacelnik and T. Martin for comments on the manuscript; and
L. Hamilton, B. Bair, L. Cargill, S. Everding, D. Hansen, M. Magrath and C. Morrill for help in the field.
Research was funded by the Chapman Fund, National Geographic Society, National Science Foundation,
Princeton University and Sigma Xi Society. Kananaskis Field Stations of the University of Calgary
provided support during writing.
Correspondence and requests for materials should be addressed to B.E.L. at Santa Cruz (e-mail:
lyon@biology.ucsc.edu).
Exceptional soft-tissue
preservation in a
theropod dinosaur from Italy
Cristiano Dal Sasso*& Marco Signore†‡
*Museo Civico di Storia Naturale, Corso Venezia 55, 20121 Milano, Italy
†Dipartimento di Paleontologia, Universita
`degli Studi di Napoli ‘‘Federico II’’,
Largo S. Marcellino 10, 80138 Napoli, Italy
‡Department of Geology, University of Bristol, Wills Memorial Building,
Queens Road, Bristol BS8 1RJ, UK
.........................................................................................................................
The Lower Cretaceous Pietraroia Plattenkalk (Benevento Pro-
vince, southern Italy) has been known since the eighteenth
century for its beautifully preserved fossil fishes. During Albian
time (about 113 Myr ago1), deposition of fine marly limestone in a
shallow lagoonal environment, affected by cyclic periods of low
oxygen levels2, led to exceptional preservation of soft tissue in a
Nature © Macmillan Publishers Ltd 1998
8
letters to nature
384 NATURE
|
VOL 392
|
26 MARCH 1998
Figure 1 The holotype of Scipionyx samniticus, gen. et sp. nov., fossilized in a
beige limestone from the Lower Cretaceous (Albian) of Pietraroia (Benevento,
southern Italy). Scale bar, 2cm. Courtesy of the Soprintendenza Archeologica,
Salerno.
Figure 3 Close-up of the skull of Scipionyx. Scale bar, 1 cm. Courtesy of the Soprintendenza Archeologica, Salerno.
Nature © Macmillan Publishers Ltd 1998
8
letters to nature
NATURE
|
VOL 392
|
26 MARCH 1998 385
juvenile theropod. The specimen, diagnosed here as Scipionyx
samniticus gen. et sp. nov., is the first dinosaurever to be found in
Italy. The fossil has been mentioned previously in two brief
notes3,4 and generally examined in a doctoral thesis5. Here we
report the full preparation of the specimen which shows details of
soft anatomy never seen previously in any dinosaur. The pre-
servation is better than in other lagersta
¨tten (conservative
deposits)6where theropod soft tissue has been reported, such as
the Santana Formation of Brazil7and the Yixian Formation of
China8. Despite this, there is no evidence of feathers or any other
integumentary remnants in the Italian specimen. Scipionyx
represents a new maniraptoriform theropod. Its discovery is
remarkable considering also the scarcity of juvenile theropod
dinosaurs in the fossil record.
The skeleton of the Pietraroia dinosaur, 237-mm long from the
tip of premaxilla to the last (ninth) preserved caudal vertebra, lies on
its left side (Figs 1, 2), in nearly perfect anatomical articulation.
Although the head is upturned with respect to the position in life,
Figure 2 Scipionyx samniticus gen. et sp. nov. Sketch of the skeleton shown in
Fig. 1. Abbreviations: ab, anterior blade of ilium; ac, acromion; act, acetabulum;
aofe, antorbital fenestra; ar, abdominal rib; at, atlas; ax, axis; bt, biceps tubercle; C,
cervical vertebra; Cc, cervical centrum; cf, coracoid foramen; cfl, M. caudifemor-
alis longus; chv, chevron bones; cn, cnemial crest; co, coracoid; cr,cervical rib; D,
dorsal vertebra; Dc, dorsal centrum; dc, distal carpal; dp, diapophysis; dpc,
deltopectoral crest; dr, dorsal rib; emfe, external mandibular fenestra; en, external
naris; ep, epipophysis; f, furcula; fe, femur; fi, fibula; ft, flexor tubercle; g, gastralia;
gl, glenoid fossa; gt, greater trochanter; h, head of humerus; hc, horny claw; hu,
humerus; hy, hyoid; hyp, hyposphene–hypantrum; if, ischiadic foot; il, ilium; im,
ischiadic musculature; int, intestine; ip, ischiadic peduncle; itfe, infratemporal
fenestra; liv, liver;Imf, large muscular fibres; lt, lesser trochanter; mc, metacarpal;
ns, neural spine; ofe, orbital fenestra; op, olecranon process; pb, posterior blade
of ilium; pem, pectoral musculature; pf, pubic foot; pp, pubic peduncle; pu, pubis;
pz, pre-postzygapophyses; Q, caudal vertebra; ra,radius; rae, radiale; sc, scapula;
Sc, sacral centrum; Sn, sacral neural arch; sr, sacral rib; ss, sagittal suture; st,
sternal plate; stfe, supratemporal fenestra; ti, tibia; tp, transverse process; tra,
trachea; ul, ulna; I–III, first to third digits, 1 –4, first to fourth phalanxes. Left-side
elements are in parentheses. Scale bar, 2 cm.
Figure 4 Sketch of the skull of Scipionyx shown in Fig. 3. Abbreviations: an,
angular; aofe, antorbital fenestra; bpt, basipterygoid; bs, basisphenoid; ect,
ectopterygoid; emfe, external mandibular fenestra; en, external naris; f, frontal;
idp, interdental plates; if, inner (orbital) wall of frontal; im, inner (lingual) wall of
maxillary; ipa, inner prearticular; ipo, inner (orbital) wall of postorbital; itfe, infra-
temporal fenestra; j, jugal; l, lachrymal; ls, laterosphenoid; lv, lachrymal vacuity; m,
maxillary; mg, meckelian groove; ms, mandibular symphysis; mxfe, maxillary
fenestra; n, nasal; ofe, orbital fenestra; os, orbitosphenoid; p, parietal; pa,
prearticular; pal, palatine; pf, parietal flange; pm, premaxillary; po, postorbital;
pop, paroccipital process; prf, prefrontal; prfe, promaxillary fenestra; ps,
parasphenoid; pt, pterygoid; q, quadrate; qj, quadratojugal; sa, surangular; sc,
sclerotic plates; sd, supradentary; so, supraoccipital; sp, splenial; sq, squamosal;
ss, sagittal suture; stfe, supratemporal fenestra; tpor,transverse postorbital ridge;
v, vomer; 4, fourth maxillary tooth, Left-side elements are in parentheses. Scale
bar,1 cm.
Nature © Macmillan Publishers Ltd 1998
8
letters to nature
386 NATURE
|
VOL 392
|
26 MARCH 1998
there is no opisthotonic condition9in the neck. The hindlimbs are
missing distal to the proximal epipodials, as are most of the tail and
most of the second right manual claw.
Theropoda
Tetanurae
Coelurosauria
Maniraptoriformes
Scipionyx samniticus gen. et sp. nov.
Etymology. Scipio (Latin male name): dedicated to Scipione
Breislak, who first described the Pietraroia Plattenkalk, and Publius
Cornelius Scipio (nicknamed Africanus), consul militaris of the
Roman Army, who fought in the Mediterranean area; onyx (Greek):
claw; samniticus (Latin): of the Samnium, ancient name of the
region including the Benevento Province.
Holotype. Nearly complete, articulated skeleton, housed at the
Soprintendenza Archeologica, Salerno.
Horizon and locality. Lower Cretaceous (Albian) of the Pietraroia
Plattenkalk (Benevento Province, southern Italy).
Diagnosis. Referable to Theropoda10– 12 for the synapomorphic
presence of denticulate teeth, intramandibular joint, straplikescapular
blade, distal carpal 1 clasping metacarpals I and II, manus with
digits IV and V absent and with elongate penultimate phalanges,
booted pubis. Referable to Coelurosauria11,12 on the basis of the
derived presence of jugal participation in the antorbital fenestra and
metacarpal I being one-third the length of metacarpal II; more
primitive than other coelurosaurs in retaining stout lachrymal and
ischial foot. Referable to Maniraptoriformes12,13 on the basis of the
derived presence of third antorbital fenestra, elongate cervical
prezygapophyses, forelimb/presacral ratio of 0.75, ulna bowed
posteriorly, semilunate carpal, and slender metacarpal III. Differs
from all other Maniraptoriformes in the unique possession of an
accessory transverse postorbital ridge at fronto–parietal contact,
and by the compressed nature of the radiale and semilunate carpal;
differs also in the primitive retention of large prefrontal, pro-
nounced scapular acromion, and rounded coracoid caudal end.
The body proportions indicate that this animal is little morethan
a hatchling14–16. The skull/presacral ratio (0.48) is higher than in any
known adult theropod, including Tyrannosaurus17; moreover, the
antorbital region is short, and the orbit is large and circular. Many
skeletal elements (scapulo–coracoid, sternal plates, sacral verte-
brae) are unfused18, and several neural arches are separate from their
centra. The symmetry of tooth development in both maxillary rami
suggests that the first tooth replacement had not occurred; further-
more, the low denticle count may be related to juvenile age14,19.
A combination of characters that usually identify different
clades11,12 is present in the Italian theropod. The forelimb ratios
and most elements of the skull (Figs 3, 4) resemble features of
dromaeosaurids17,20,21. Among them are the following derived char-
acters: sloping postorbital region; quadrate with a single head
Figure 5 Close-up of the abdomen of Scipionyx, showing the perfectly fossilized
intestine (left) and a reddish macula that might represent the remains of the liver
(right). Scale bar,1 cm. Courtesy of the Soprintendenza Archeologica, Salerno.
Nature © Macmillan Publishers Ltd 1998
8
letters to nature
NATURE
|
VOL 392
|
26 MARCH 1998 387
articulating exclusively with the squamosal; paroccipital processes
distally slightly twisted postero–dorsally; maxillary fenestra dor-
sally displaced; palatine pneumatization; alignment of dentary
foramina into two rows, not in grooves; and splenial emerging
externally on the lateral surface of the mandible. Other characters,
such as the small, L-shaped quadratojugal with equal rami, low
cervical neural spines, and the barely propubic pelvis, are not
dromaeosaurid, but appear synapomorphic with the
Troodontidae22. There are also ornithomimid-like, plesiomorphic
features, clearly differentiating the pelvis of Scipionyx from both the
dromaeosaurid and the troodontid pattern (for example, the ilium
is posteriorly truncated, and the ischium is three-quarters of the
pubic length, with a forward-pointing foot12,23). Moreover,
characters such as the L-shaped lachrymal, fan-like coracoid,
feeble development of the fourth trochanter, and slender and slightly
curved chevrons, resemble a more generalized coelurosaurian
bauplan9,11,24.
The mosaic of characters does not allow attribution of this new
genus to any known theropod family. But the phylogenetic relation-
ships of Scipionyx must undoubtedly be searched for within the
Maniraptoriformes, as it shares at least six unambiguous synapo-
morphies with that clade12,13 (see Diagnosis).
A unique, striking feature of the specimen is the preservation of
soft parts (Figs 1, 5). Muscles are present in the pectoral area, with
scattered acicular fibres clearly visible under ×50 magnification. At
the tail base, a fascium with at least three different arrangements of
fibrae longae possibly represents part of the M. caudifemoralis
longus25,26. Most of the intestine (tenuis27), 5.22-mm average
diameter) is positioned further forwards than it is generally thought
to be25,28, whereas the colon27 passes through the pelvic canal, close
to the vertebral column, and ends just above the ischiadic foot. The
gut is surprisingly short and deep in section, suggesting a high
absorbtion rate. Its muscular wall has transverse folds, which are
sometimes anastomized. Immediately above the furcula, there
appear to be some tracheal rings. A large, reddish, well delimited
haematitic halo is tentatively interpreted as liver traces, mainly
because of its post-sternal location.
The gastralia, still in life position, allow estimation of the
abdominal depth and reveal their contribution to an effective
support for the posterior intestinal tract. The presence of a furcula
in this articulated specimen eliminates every doubt about the
interpretation of similar structures in other theropods29,30.M
Received 17 September 1997; accepted 9 February 1998.
1. Bravi, S. & De Castro, P. The Cretaceousfossil fishes level of Capo d’Orlando, near Castellammare di
Stabia (NA): biostratigraphy and depositional environment. Mem. Sci. Geol. 47, 45–72 (1995).
2. Bravi, S. Contributo allo studio del giacimento ad ittioliti di Pietraroja (Benevento) (Thesis, Dip. Geol.
Univ. Napoli ‘‘Federico II’’, 1987).
3. Leonardi, G. & Teruzzi, G. Prima segnalazione di uno scheletro fossile di dinosauro (Theropoda,
Coelurosauria) in Italia (Cretacico di Pietraroia, Benevento). Paleocronache 1993, 7–14 (1993).
4. Leonardi, G. & Avanzini, M. Dinosauri in Italia. Le Scienze (Quaderni) 76, 69 –81 (1994).
5. Signore, M. Il teropode del Plattenkalk della Civita di Pietraroia (Cretaceo inferiore, Bn) (Thesis, Dip.
Paleont. Univ. Napoli ‘‘Federico II’’, 1995).
6. Seilacher, A. Begriff und Bedentung der Fossil-Lagersta
¨tten. N. Jb. Geol. Pala
¨ont. Mh. Jahr.1970, 34 –39
(1970).
7. Kellner, A. Fossilized theropod soft tissue. Nature 379, 32 (1996).
8. Ji, Q. & Ji, S. On discovery of the earliest bird fossil in China and the origin of birds. Chinese Geol. 233,
30–33 (1996).
9. Ostrom, J. H. The osteology of Compsognathus longipes Wagner. Zitteliana 4, 73–118 (1978).
10. Benton, M. J. in The Dinosauria (eds Weishampel, D. B., Dodson, P. & Osmo
´lska, H.) 11– 30 (Univ.
California, Berkeley, 1990).
11. Gauthier, J. in Mem. Calif. Acad. Sci. (ed. Padian, K.) 8, 1–55 (1986).
12. Holtz, T. R. Jr The phylogenetic position of the Tyrannosauridae: implications for theropod
systematics. J. Paleontol. 68, 1100–1117 (1994).
13. Holtz, T. R. Jr Phylogenetic taxonomyof the Coelurosauria (Dinosauria: Theropoda). J. Paleontol. 70,
536–538 (1996).
14. Norell, M. A. et al. A theropod dinosaur embryo and the affinities of the Flaming Cliffs dinosaur eggs.
Science 266, 779–782 (1994).
15. Colbert, E. H. in Dinosaur Systematics (eds Carpenter, K. & Currie, P. J.) 81– 90 (Cambridge Univ.
Press, 1990).
16. Molnar, R. E. in Dinosaur Systematics (eds Carpenter, K. & Currie, P. J.) 71–79 (Cambridge Univ.
Press, 1990).
17. Ostrom, J. H. Osteology of Deinonychus antirrhopus, an unusual theropod from the Lower Cretaceous
of Montana. Bull. Peabody Mus. Nat. Hist. 30, 1–165 (1969).
18. Currie, P. J. & Zhao, X. A new carnosaur (Dinosauria, Theropoda) from the Jurassic of Xinjiang,
People’s Republic of China. Can. J. Earth Sci. 30, 2037–2081 (1993).
19. Currie, P. J. et al. in Dinosaur Systematics (eds Carpenter, K.& Currie, P. J.) 107–125 (Cambridge Univ.
Press, 1990).
20. Currie, P. J. New information on the anatomy and relationships of Dromaeosaurus albertensis
(Dinosauria: Theropoda). J. Vert. Paleontol. 15, 576–591 (1995).
21. Witmer, L. M. & Maxwell, W. D.The skull of Deinonychus (Dinosauria: Theropoda): new insights and
implications. J. Vert. Paleontol. 16, 73A (1996).
22. Russell, D. A. & Dong, Z. A nearly complete skeleton of a new troodontid dinosaur from the Early
Cretaceous of the Ordos Basin, Inner Mongolia, People’s Republic of China. Can. J. Earth. Sci. 30,
2163–2173 (1993).
23. Barsbold, R. & Osmo
´lska, H. in The Dinosauria (eds Weishampel, D.B., Dodson, P. & Osmo
´lska, H.)
225–244 (Univ. California, Berkeley, 1990).
24. Norman, D.B. in The Dinosauria (eds Weishampel,D. B., Dodson, P.& Osmo
´lska, H.) 280– 305 (Univ.
California, Berkeley, 1990).
25. Paul, G. S. Predatory Dinosaurs of the World 1– 464 (Simon & Schuster, 1988).
26. Gatesy, S. M. in Functional Morphology in Vertebrate Paleontology (ed. Thomason, J.) 219– 234
(Cambridge Univ. Press, 1995).
27. Guibe
´, J. Traite
´de Zoologie 14-II (ed. Grasse
´, P. P.) 521–548 (Masson, 1970).
28. Wellnhofer, P. in The Beginning of Birds (eds Hecht, M. K., Ostrom, J. H., Viohl, G. & Wellnhofer, P.)
113–122 (Freunde des Jura-Museums, Eichsta
¨tt, 1985).
29. Bryant, H. N. & Russell, A. P. The occurrence of clavicles within Dinosauria: implications for the
homology of the avian furcula and the utility of negative evidence. J. Vert. Paleontol. 13, 171–184
(1993).
30. Norell, M. A. et al. A Velociraptor wishbone. Nature 389, 447 (1997).
Acknowledgements. We thank P. J. Currie and M. J. Benton for critical revision of the manuscript;
C. Barbera, L. Chiappe, P. Makovicky, M. Norell, M. Novacek, E. Koppelhus, E. Nicholls, A. Kotsakis,
D. Maxwell, R. Molnar, G. Pasini, E. Signore, G. Todesco, and L. Witmer; G. Leonardi for his
encouragement; S. Rampinelli for the superb preparation of the specimen; G. Teruzzi, Dinosaur Project
coordinator; and G. Tocco for allowing us to study the specimen. Photographs are by L. Vitola; drawings
are by F. Fogliazza.
Correspondence and requests for materials should be addressed toC.D.S. (e-mail: cdalsasso@yahoo.com).
Somatosensorydiscrimination
based on cortical
microstimulation
Ranulfo Romo, Adria
´n Herna
´ndez, Antonio Zainos
& Emilio Salinas
Instituto de Fisiologı
´a Celular, Universidad Nacional Auto
´noma de Me
´xico,
04510 Me
´xico DF, Me
´xico
.........................................................................................................................
The sensation of flutter is produced when mechanical vibrations
in the range of 5– 50 Hz are applied to the skin1– 3. A flutter
stimulus activates neurons in the primary somatosensory cortex
(S1) that somatotopically map to the site of stimulation4,5. A
subset of these neurons— those with quickly adapting properties,
associated with Meissner’s corpuscles—are strongly entrained by
periodic flutter vibrations, firing with a probability that oscillates
at the input frequency1,6. Hence, quickly adapting neurons pro-
vide a dynamic representation of such flutter stimuli. However,
are these neurons directly involved in the perception of flutter?
Here we investigate this in monkeys trained to discriminate the
difference in frequency between two flutter stimuli delivered
sequentially on the fingertips1,7. Microelectrodes were inserted
into area 3b of S1 and the second stimulus was substituted with a
train of injected current pulses. Animals reliably indicated
whether the frequency of the second (electrical) signal was
higher or lower than that of the first (mechanical) signal, even
though both frequencies changed from trial to trial. Almost
identical results were obtained with periodic and aperiodic
stimuli of equal average frequencies. Thus, the quickly adapting
neurons in area 3b activate the circuit leading to the perception of
flutter. Furthermore, as far as can be psychophysically quantified
during discrimination, the neural code underlying the sensation
of flutter can be finely manipulated, to the extent that the
behavioural responses produced by natural and artificial stimuli
are indistinguishable.
Two monkeys (Macaca mulatta) were trained in a standard
discrimination task7in which two mechanical vibrations, termed
base and comparison, are delivered in each trial (Fig. 1). The
monkeys learned to indicate whether the comparison stimulus
