letters to nature
16. Gaffney, E. S. Cranial morphology of the European Jurassic turtles Portlandemys and Plesiochelys. Bull.
Am. Mus. Nat. Hist. 157, 489–543 (1976).
17. Gaffney, E. S. Comparative cranial morphology of recent and fossil turtles. Bull. Am. Mus. Nat. Hist.
164, 65–375 (1979).
18. Gaffney, E. S. The comparative osteology of the Triassic turtle Proganochelys. Bull. Am. Mus. Nat. Hist.
194, 1–263 (1990).
19. Schumacher, G.-H. Die Kopf- und Halsregion der Leder-schildkröte Dermochelys coriacea (Linnaeus
1976). Abhandl. Akad. Wissensch. 1972, 1–60 (1973).
20. Schumacher, G.-H. in Biology of the Reptilia. 4 (eds Gans, C. & Parsons, T. S.) 101–199 (Academic,
New York, 1973).
21. Rieppel, O. The skull of the Upper Jurassic cryptodire turtle Thalassemys, with a reconsideration of the
chelonian braincase. Palaeontogr. A 171, 105–140 (1980).
22. Zangerl, R. The vertebrate fauna of the Selma Formation of Alabama. Part 5. An advanced chelonioid
sea turtle. Fieldiana Geol. Mem. 3, 61–277 (1960).
macronutrients or trace metals into the surface mixed layer from
UCDW at the Southern Boundary should increase regional primary
production, enhance secondary production (that is, production of
krill) and attract cetaceans and other foraging apex predators. In
general, nutrients are not considered to be limiting for phytoplankton growth in Antarctic waters4 and local iron enrichment may be
an important factor that determines the spatial variability in
phytoplankton production5. However, the concentrations of iron
and other trace elements in UCDW and near the Southern Boundary
Supplementary information is available on Nature’s World-Wide Web site (http://www.nature.com) or
as paper copy from Mary Sheehan at the editorial office of Nature.
Acknowledgements. I thank F. Bacchia for field collection of the Santana turtles; E. S. Gaffney, P. E.
Meylan and T. Hirayama for comments on manuscript; E. Hooks III for advice on protostegid
morphology; D. B. Brinkman for comments on primitive eucryptodires; and N. Kohno for advice on
the methodology of phylogenetic analysis. This work was partially supported by grants from the Teikyo
Heisei University (formerly Teikyo University of Technology).
Correspondence and requests for materials should be addressed to R.H. (e-mail: [email protected]).
Ecological importance of the
Southern Boundary of the
Antarctic Circumpolar Current
Cynthia T. Tynan
Research Associate of the National Research Council, National Marine Mammal
Laboratory, NOAA, 7600 Sand Point Way NE, Seattle, Washington 98115, USA
.........................................................................................................................
The Southern Ocean surrounds the Antarctic continent and
supports one of the most productive marine ecosystems. Migratory and endemic species of whales, seals and birds benefit from
the high biomass of their principal prey, krill (Euphausia superba)
and cephalopods, in this area. Most species of baleen whales and
male sperm whales in the Southern Hemisphere migrate between
low-latitude breeding grounds in winter and highly productive
Antarctic feeding grounds in summer. Here I show the importance of the southernmost reaches of the strongest ocean current,
the Antarctic Circumpolar Current (ACC), to a complex and
predictable food web of the Southern Ocean. The circumpolar
distributions of blue, fin and humpback whales from spring to
midsummer trace the non-uniform high-latitude penetration of
shoaled, nutrient-rich Upper Circumpolar Deep Water, which is
carried eastward by the ACC. The poleward extent of this water
mass delineates the Southern Boundary1 of the ACC and corresponds not only to the circumpolar distributions of baleen whales,
but also to distributions of krill and to regions of high, seasonally
averaged, phytoplankton biomass. Sperm whales, which feed on
cephalopods2, also congregate in highest densities near the Southern Boundary. The association of primary production, Krill, and
whales with the Southern Boundary, suggests that it provides
predictably productive foraging for many species, and is of critical
importance to the function of the Southern Ocean ecosystem.
The ACC is dominated by a thick layer of warm, saline, oxygenpoor and macronutrient-rich water, Circumpolar Deep Water
(CDW), which originates at low latitudes, shoals southwards, and
is eventually entrained in the surface mixed layer1,3. Upper Circumpolar Deep Water (UCDW)1,3 is the only water mass that is found
exclusively in the ACC1. At its poleward edge, UCDW lies at depths
near 200–500 m, where wind-induced divergence and upwelling
bring high concentrations of phosphate, nitrate, and silicate to the
Antarctic Surface Water3. The southern end of the characteristic
signal of UCDW is a water-mass boundary which constitutes a
reasonable poleward extent of the ACC; this feature has been named
the Southern Boundary1.
The upward flux and entrainment of high concentrations of
708
Land/< 0.05
no data
0.1
0.2 0.4 0.6 0.8 1.0
1.2
1.4
1.6
1.8
2.0 5.0 >5.0 Pigment
concentration
(mg per m3)
Figure 1 Annual coastal zone colour scanner (CZCS) pigment concentration,
averaged from data from October 1978 to June 1986 (ref. 4), in relation to the
location of the Southern Boundary of the ACC1 (white line).
30º
0º
30º
60º
60º
90º
90º
120º
120º
5 0º
3 5º
150º
W180º E
150º
6
Figure 2 Distribution of principal concentrations of krill in relation to the East
Wind Drift and Weddell Drift (dashed lines), Polar Front (black line) and Southern
Boundary1 (red line). Principal concentrations of krill are shown as encircled black
circles.
Nature © Macmillan Publishers Ltd 1998
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letters to nature
have not been examined. The Antarctic circumpolar distribution of
phytoplankton pigment4 shows that regions of higher primary
productivity coincide with the Southern Boundary (Fig. 1).
Where the Southern Boundary occurs close to the Antarctic continent (Southern Indian Ocean, 408–1508 E, and the southeast
Pacific Ocean, 1108 W to the Drake Passage), the highest phytoplankton pigment is confined to a narrower band along the continent. Conversely, where topography steers the Southern Boundary
northwards away from the continent (east of the Antarctic
Peninsula along the Weddell–Scotia Confluence, east of the Adelie
Coast and north of the Ross Sea, and along the eastern flank of the
Kerguelen Plateau), zones of higher productivity extend to much
lower latitudes (Fig. 1).
The asymmetrical circumpolar distribution of krill6 also matches
the asymmetry in the poleward extent of the Southern Boundary
between ocean basins (Fig. 2). Despite regional-scale temporal and
spatial variability in the recruitment and abundance of krill7,8, the
large-scale circumpolar pattern of principal krill concentrations still
aligns with the Southern Boundary (Fig. 2). The duration and
extent of ice cover has been linked to the spawning and recruitment
success of krill7. Therefore, linkages between the Southern Boundary
and the circumpolar pattern of sea ice should have a synergistic
effect on krill distribution. Although the distribution of krill has
been related to the prevailing surface currents6, the link between krill
distribution and the Southern Boundary suggests the influence of
shoaled UCDW. Eggs of krill are released at the surface, sink to
deeper levels of warmer CDW, and hatch at depth9. The reproductive strategy of krill has evolved in response to CDW and the thermal
structure, which enhances larval survival10. Therefore, the Southern
Boundary should have an important effect on the distribution,
development and feeding success of krill.
The broad, circumpolar distributions of whales from spring to
midsummer also reflect the non-uniform high-latitude penetration
of UCDW. Whales can occur as far south as the retreating
ice edge11,12; however, the highest concentrations of blue whales
0o
a
90o W
40o
50o
(Balaenoptera musculus), humpback whales (Megaptera novaeangliae) (Fig. 3) and fin whales (Balaenoptera physalus) coincide with
the Southern Boundary in late spring and early summer. In
December, the edge of the receding seasonal ice is near the Southern
Boundary and the distribution of these three species of baleen
whales aligns with both of these features. By January, however, when
the ice has retreated closer to the continent, the highest densities of
whales in some sectors of the Southern Ocean remain in ice-free
areas near the Southern Boundary (Fig. 3). This may reflect
processes at the Southern boundary as well as the development of
the productive marginal ice zone13 as the ice recedes. This distribution of the whales is particularly apparent in the South Atlantic from
308 W to 408 E, near the Kerguelen Plateau at 908 E, and in the
South Pacific between 1508 E and 1508 W in regions where the
Southern Boundary is further from the continent. Between the
Weddell and Ross Gyres, where the Southern Boundary and the
receding ice edge are closer to the Antarctic continent, higher
densities of these three species of baleen whales also occur closer
to the continent (408–1608 E; 608–1208 W). Past the eastern ends of
the subpolar cyclones, near 308 E (ref. 14) and 1308 W (ref. 15), the
ACC shifts southward, bringing CDW close to the Antarctic Shelf
Waters1. The distributions of whales during December and January
also show this pattern of higher-latitude penetration in the regions
between the Weddell and Ross Gyres (Fig. 3); presumably the whales
are responding to the distribution of krill (Fig. 2) and the proximity
of the ACC to the continental slope. This pattern shows that the
Southern Boundary serves as a predictably productive foraging
location for several months during the southward migration of
the whales. As the pack ice retreats during the summer, with the
continued development of the productive marginal ice-edge zone13,
whales penetrate south of the Southern Boundary, approaching
closer to the continent by February and March.
The circumpolar distribution of sperm whales (Physeter macrocephalus) also follows the Southern Boundary (Fig. 4). Sperm
whales concentrate at higher latitudes in the Indian Ocean than in
8
b
90o E
90oW
0o
40o
50o
180o
1800
Frequency of grid cells
(with actual class intervals)
Class intervals
1
Median
3 2 median
7 2 median
Maximum
1-29 whales per cell
30-87
88-203
204-435 (633)
200 400 600 800
90oE
Frequency of grid cells
(with actual class intervals)
Actual catch
4,490 whales
11,139
19,240
17,998
52,867 = total catch
Class intervals
1
Median
3 × median
7 × median
Maximum
1-8 whales per cell
9-24
25-56
57-120 (250)
200 400 600 800
Actual catch
522 whales
1,264
1,923
3,837
7,546 = total catch
Figure 3 Distribution of whale catches. a, Blue whale, and b, humpback whale
monthly extent of sea-ice coverage (blue) for January of 1979–1987 (ref. 19). Grid
catches during January of 1931/1932–1966/1967 and 1931/1932–1962/1963,
size of the whale data is 18 latitude 3 28 longitude.
respectively17, in relation to the Southern Boundary1 (red line) and the mean
NATURE | VOL 392 | 16 APRIL 1998
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letters to nature
40 o
30 o
20 o
10 o 0 o
10 o 20 o
30 o
40 o
50 o
50 o
60 o
60 o
70
o
70
o
80
o
80
o
90 o
90 o
100 o
100 o
110 o
110 o
Number of
Sperm whales
Sperm whales per eff. c.dw
120 o
130 o
1–50
0.01– 0.50
100
0.51–1.00
200
1.01–1.50
300
over 1.50
140 o
150 o 160 o 170 o 180 o 170 o 160 o
120 o
130 o
150 o
140 o
Figure 4 Distribution of sperm whale catches during the 1950s (ref.18) in relation
to the Southern Boundary1 (red line). Catch data are gridded 58 latitude 3
108 longitude, as total numbers (circles) and total catch per effective catcher’s
day’s work (triangles).
2. Clarke, M. R. Cephalopoda in the diet of sperm whales of the Southern Hemisphere and their bearing
on sperm whale biology. Discov. Rep. 37, 1–324 (1980).
3. Sievers, H. A. & Nowlin, W. D. Jr The stratification and water masses at Drake Passage. J. Geophys. Res.
89, 10489–10514 (1984).
4. Comiso, J. C. et al. Coastal zone color scanner pigment concentrations in the Southern Ocean and
relationships to geophysical surface features. J. Geophys. Res. 98, 2419–2451 (1993).
5. de Baar, H. J. W. et al. Importance of iron for plankton blooms and carbon dioxide drawdown in the
Southern Ocean. Nature 373, 412–415 (1995).
6. Marr, J. W. S. The natural history and geography of the Antarctic krill (Euphausia superba Dana).
Disov. Rep. 32, 33–464 (1962).
7. Siegel, V. & Loeb, V. Recruitment of Antarctic krill Euphausia superba and possible causes for its
variability. Mar. Ecol. Prog. Ser. 123, 45–56 (1995).
8. Priddle, J. et al. in Antarctic Ocean and Resources Variability (ed. Sahrhage, D.) 169–182 (Springer,
Berlin, 1988).
9. Laws, R. M. The ecology of the Southern Ocean. Am. Sci. 73, 26–40 (1985).
10. Hofmann, E. E. et al. Models of the early life history of Euphausia superba—Part I. Time and
temperature dependence during the descent-ascent cycle. Deep-Sea Res. 39, 1177–1200 (1992).
11. Ribic, C. A., Ainley, D. G. & Fraser, W. R. Habitat selection by marine mammals in the marginal ice
zone. Ant. Sci. 3, 181–186 (1991).
12. de la Mare, W. K. Abrupt mid-twentieth-century decline in Antarctic sea-ice extent from whaling
records. Nature 389, 57–59 (1997).
13. Smith, W. O. Jr. & Nelson, D. M. Importance of ice edge phytoplankton production in the Southern
Ocean. BioScience 36, 251–257 (1986).
14. Orsi, A. H., Nowlin, W. D. Jr. & Whitworth, T. III On the circulation and stratification of the Weddell
Gyre. Deep-Sea Res. I 40, 169–203 (1993).
15. Locarnini, R. A. Water Masses and Circulation in the Ross Gyre and Environs (thesis, Texas A&M Univ.
1994).
16. Rodhouse, P. G. & White, M. G. Cephalopods occupy the ecological niche of epipelagic fish in the
Antarctic Polar Frontal Zone. Biol. Bull. 189, 77–80 (1995).
17. Mizroch, S. A., Rice, D. W. & Larson, S. W. Distribution of Rorquals in the Southern Ocean: An Atlas
based on Pelagic Catch Data (Fishery Bull., in the press).
18. Holm, J. L. & Jonsgård, Å. Occurrence of the sperm whale in the Antarctic and the possible influence of
the moon. The Norwegian Whaling Gazette 4, 161–182 (1959).
19. Gloersen, P. et al. Arctic and Antarctic Sea Ice, 1978–1987: Satellite Passive-Microwave Observations and
Analysis (NASA SP-511) (NASA, Washington DC, 1992).
Acknowledgements. I thank D. P. DeMaster, R. L. Gentry, G. L. Kooyman, D. G. M. Miller, A. H. Orsi and
J. Priddle for review of the manuscript, and A. H. Orsi for discussions and for providing the coordinates of
the Southern Boundary of the ACC.
Correspondence and requests for materials should be addressed to C.T.T. (e-mail: [email protected]).
the South Atlantic Ocean and track the increasing southward
penetration of the Southern Boundary between 208–608 E. Where
the Southern Boundary occurs close to the Antarctic continent,
such as in the Southern Indian Ocean, higher densities of sperm
whales were historically found closer to the continent (Fig. 4).
Regions in which sperm whales occurred in greater numbers in the
1950s, such as the South Sandwich Trench and northwest of
Enderby Land, lie along or north of the Southern Boundary
(Fig. 4). Therefore, male sperm whales seem to migrate southward
as far as the poleward extent of UCDW. This suggests that the
shoaling of UCDW may also affect the vertical movements and
availability of squid, the preferred prey of sperm whales.
The presence of balaenopterids and sperm whales at the Southern
Boundary indicates that processes there may enhance the availability of both krill and cephalopods. This suggests a trophic
structure at the Southern Boundary that is different from the
open-ocean trophic system of the Polar Frontal Zone in the Scotia
Sea, where krill are absent and fishes are replaced by squid16.
Pinnipeds and birds should also benefit from this complex and
predictably productive feature. The Southern Boundary is identified
here as a critical trophic structure in the function of the Southern
Ocean ecosystem, determining the broad circumpolar distribution
of productivity and the resulting cascade of trophic dynamics. M
.........................................................................................................................
Methods
Monthly catch data from whaling operations in the Southern Ocean from 1931
to 1962 (ref. 17) were used to delineate the historical monthly distributions of
blue, fin and humpback whales. Norwegian catch data of sperm whales from
four seasons during the 1950s (ref. 18) were also analysed together with details
of the Southern Boundary1. Mean monthly coverage of the Antarctic seasonal
sea ice was obtained from satellite passive-microwave analyses for 1979–1987
(ref. 19). The whale-distribution data and the sea-ice data are not contemporary, as there are no circumpolar, synoptic, seasonal sea-ice data available for the
whaling period 1931–1962.
Received 15 October 1996; accepted 15 January 1998.
1. Orsi, A. H., Whitworth, T. III & Nowlin, W. D. Jr On the meridional extent and fronts of the Antarctic
Circumpolar Current. Deep-Sea Res. I 42, 641–673 (1995).
710
Multiple stored views and
landmark guidance in ants
S. P. D. Judd & T. S. Collett
Sussex Centre for Neuroscience, School of Biological Sciences,
Brighton BN1 9QG, UK
.........................................................................................................................
Under some circumstances, Diptera and Hymenoptera learn
visual shapes retinotopically, so that they only recognize the
shape when it is viewed by the same region of retina that was
exposed to it during learning1,2. One use of such retinotopically
stored views is in guiding an insect’s path to a familiar site3–5.
Because the retinal image of an object changes with viewing
distance and (sometimes) direction, a single stored view may be
insufficient to guide an insect from start to goal. Little, however, is
known about the number of views that insects store. Here we show
that wood ants take several ‘snapshots’ of a familiar beacon from
different vantage points. An ant leaving a newly discovered food
source at the base of a landmark performs a tortuous walk back to
its nest during which it periodically turns back and faces the
landmark. The ant, on revisiting the familiar landmark, holds the
edges of the landmark’s image steady at several discrete positions
on its retina. These preferred retinal positions tend to match the
positions of landmark edges that the ant captured during its
preceding ‘learning walks’.
To investigate the possibility that wood ants (Formica rufa) store
multiple views, we analysed their behaviour as they approached a
cone. Our first step was to demonstrate that ants learn to distinguish
between upright and inverted cones. An ant that had been trained to
find sucrose close to either an upright or an inverted cone was
presented with a choice between the two cones placed ,12 cm apart
and ,40 cm from the ant (Fig. 1a). The ant approached the pair
veering from one to the other. At a mean distance of 15.8 cm
(s:d: ¼ 7:2 cm, n ¼ 76) from the cones, it tended to select the
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