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DOI: 10.1126/science.1211437 , 1699 (2011);334 Science

, et al.John R. Hutchinson Evolution of Elephant ''Sixth Toes'' From Flat Foot to Fat Foot: Structure, Ontogeny, Function, and

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in the Doushantuo fossils [for example, opalinids are multinuclear (32)]. Only volvocalean em- bryos show so many rounds of palintomy, but the resulting blastomeres are connected by a system of cytoplasmic bridges (35) that are not present in the fossils. The combination of palintomy with- in a multilayered cyst wall and peanut-shaped germination stages as seen in the fossils conforms to the pattern seen in nonmetazoan holozoans; nonetheless, there are no discrete characters in the Doushantuo fossils that are uniquely holozoan. The “animal embryos” likely represent nonmeta- zoan holozoans or possibly even more distant eukaryote branches.

References and Notes 1. S. Xiao, Y. Zhang, A. Knoll, Nature 391, 553

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1 (2004). 4. J.-Y. Chen et al., Science 312, 1644 (2006). 5. J. W. Hagadorn et al., Science 314, 291 (2006). 6. L. Yin et al., Nature 446, 661 (2007). 7. P. A. Cohen, A. H. Knoll, R. B. Kodner, Proc. Natl. Acad.

Sci. U.S.A. 106, 6519 (2009). 8. J.-Y. Chen et al., Proc. Natl. Acad. Sci. U.S.A. 106, 19056

(2009). 9. J. V. Bailey, S. B. Joye, K. M. Kalanetra, B. E. Flood,

F. A. Corsetti, Nature 445, 198 (2007). 10. E. C. Raff et al., Proc. Natl. Acad. Sci. U.S.A. 105, 19360

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F. A. Corsetti, Nature 446, E10 (2007) Reply. 18. S. Xiao, J. W. Hagadorn, C. Zhou, X. Yuan, Geology 35,

115 (2007). 19. P.-J. Liu, C.-Y. Yin, S.-M. Chen, F. Tang, L.-Z. Gao,

Acta Geosci. Sin. 30, 457 (2009). 20. Z. Yin et al., Precambr. Res., published online 9 September

2011 (10.1016/j.precamres.2011.08.011). 21. A. Rose, in Cell Division Control in Plants, D. P. S. Verma,

Z. Hong, Eds. (Springer, Heidelberg, 2007), pp. 207–230.

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23. K. V. Mikhailov et al., Bioessays 31, 758 (2009). 24. W. L. Marshall, M. L. Berbee, Protist 162, 33 (2011). 25. M. Pekkarinen, K. Lotman, J. Nat. Hist. 37, 1155 (2003). 26. L. Mendoza, R. A. Herr, S. N. Arseculeratne, L. Ajello,

Mycopathologia 148, 9 (1999). 27. A. Franco-Sierra, P. Alvarez-Pellitero, Parasitol. Res. 85,

562 (1999). 28. S. Raghu-Kumar, Bot. Mar. 30, 83 (1987). 29. B. S. Leander, J. Eukaryot. Microbiol. 55, 59 (2008). 30. J. T. Bonner, Integr. Biol. 1, 27 (1998). 31. M. Elbrächter, Helgol. Meersunters. 42, 593 (1988). 32. K. Hanamura, H. Endoh, Zoolog. Sci. 18, 381 (2001). 33. D. P. Molloy, D. H. Lynn, L. Giamberini, Dis. Aquat. Organ.

65, 237 (2005).

34. M. D. Herron, A. G. Desnitskiy, R. E. Michod, J. Phycol. 46, 316 (2010).

35. K. J. Green, D. L. Kirk, J. Cell Biol. 91, 743 (1981).

Acknowledgments: We thank S. Xiao, T. Cavalier-Smith, and B. Landfald for discussion; T. Hode and Z. Yue for field-work collaboration; A. Groso for assistance with the srXTM work; and P. Varvarigos and D. Elliott for the use of fig. S7. The work was supported by the Swedish Research Council, Natural Environment Research Council, Ministry of Science and Technology of China, National Natural Science Foundation of China, EU FP7, and the Paul Scherrer Institute. Figured or measured specimens are deposited at the Swedish Museum of Natural History and the Museum of Earth Science, Chinese Academy of Geological Sciences. The srXTM investigations were conducted at the X04SA and X02DA (TOMCAT) beamlines of the Swiss Light Source. The data were visualized and analyzed by using Avizo software. Data are available in the SOM. S.B. and P.C.J.D. designed the research and wrote the paper; T.H. found the nucleic structures, prepared the corresponding visualizations, and wrote the specimen descriptions in the SOM; J.A.C. found the propagule-like structures and performed taphonomic analyses and volumetric measurements; C.Y. and S.B. did the field work; C.Y. provided the additional data from Hubei; and M.S., F.M., S.B. and P.C.J.D. designed the srXTM experiments.

Supporting Online Material www.sciencemag.org/cgi/content/full/334/6063/1696/DC1 Materials and Methods SOM Text Figs. S1 to S7 Table S1 References (36–67) Movies S1 to S5

8 June 2011; accepted 16 November 2011 10.1126/science.1209537

From Flat Foot to Fat Foot: Structure, Ontogeny, Function, and Evolution of Elephant “Sixth Toes” John R. Hutchinson,1 Cyrille Delmer,2 Charlotte E. Miller,1 Thomas Hildebrandt,3

Andrew A. Pitsillides,1 Alan Boyde4

Several groups of tetrapods have expanded sesamoid (small, tendon-anchoring) bones into digit-like structures (“predigits”), such as pandas’ “thumbs.” Elephants similarly have expanded structures in the fat pads of their fore- and hindfeet, but for three centuries these have been overlooked as mere cartilaginous curiosities. We show that these are indeed massive sesamoids that employ a patchy mode of ossification of a massive cartilaginous precursor and that the predigits act functionally like digits. Further, we reveal clear osteological correlates of predigit joint articulation with the carpals/tarsals that are visible in fossils. Our survey shows that basal proboscideans were relatively “flat-footed” (plantigrade), whereas early elephantiforms evolved the more derived “tip-toed” (subunguligrade) morphology, including the predigits and fat pad, of extant elephants. Thus, elephants co-opted sesamoid bones into a role as false digits and used them for support as they changed their foot posture.

T he enlarged radial sesamoid bones of giant panda forefeet (1, 2) are classic examples of evolutionary exaptation (3, 4): co-option

of old structures for new functions. It is less widely recognized that such “sixth toes” or “false thumbs” have evolved convergently in numerous tetrapods, such as moles and frogs (5, 6). They exist in numerous mammals in a less enlarged state, variably called the prepollex/prehallux (here

called predigits), radial/tibial sesamoids, or other terms (such as falciform, accessory scaphoid, or navicular). Whether these sesamoids are ances- trally or convergently evolved in various tetra- pod clades remains to be determined. The latter seems likely, given the absence of similar sesa- moids in most fossil outgroups, yet a cartilag- inous nodular precursor cannot be excluded. Regardless, enlarged sesamoids are quite prom-

inent in both the manus (forefeet) and the pedes (hindfeet) of elephants, where they have been mistaken for sixth digits or otherwise presumed to play a role in foot support (7–9). Indeed, the recent discovery that moles have developmen- tally switched their radial sesamoid (prepollex) to a digit-like identity (10) intimates that ele- phants and other species may have done the same. Here, we report a multidisciplinary anatomical, his- tological, functional, and phylogenetic analysis (11) of the predigits in elephant feet. We hoped this would illuminate how elephants evolved their char- acteristic subunguligrade (nearly “tip-toed,” with only distal toes contacting the ground) foot posture and function, as compared with the plesiomorphic plantigrade (“flat-footed,” with wrists/ankles con- tacting the ground) foot posture in many other tetrapods.

In 1710, Blair (7) provided the first detailed osteological description of elephants, conclud- ing that they have six toes. The “sixth toes” (medialmost position; corresponding to digit zero) were later identified as the enigmatic prepollex

1Department of Veterinary Basic Sciences and Structure and Motion Laboratory, The Royal Veterinary College, Hatfield AL9 7TA and London NW1 0TU, UK. 2Department of Palaeontology, The Natural History Museum, Cromwell Road, London SW7 5BD, UK. 3Leibniz Institute for Zoo and Wildlife Research, im Forschungsverbund Berlin e.V., Postfach 601103, Berlin D-10252, Germany. 4Dental Physical Sciences, Barts and The London School of Medicine and Dentistry, Queen Mary Uni- versity of London, Mile End Road, London E1 4NS, UK.

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and prehallux (8, 9, 12) (figs. S1 to S4). Three centuries of sporadic discussion about the iden- tities of predigits in tetrapods have ensued (8, 9), sometimes returning to the question of whether they are actually atavistic digits (9, 13). Consid- ering the characteristic variability (8) and apparent mineralization late in the ontogeny of sesamoids (14), as well as their articulations (15) with meta- carpal I/tarsal I and metatarsal I (Fig. 1 and movie S1), the prepollex/prehallux of elephants must correspond to the radial/tibial sesamoids of other tetrapods. The late mineralization and confounded scientific history of predigits have tended to pre- vent their preservation, discovery, scholarly descrip- tion, and even museum exhibition. The vexing issue of the homology of elephant predigits re- mains unresolved, complicated by the specializa- tion of paenungulate outgroups (such as Sirenia and Hyracoidea).

Despite early studies, it remains unclear whether elephant predigits are never more than cartilaginous rods, as current literature assumes (8, 9, 12), or whether they become true bones at some point in ontogeny. We used a combination (11) of dissection, computed x-ray tomography (CT) scans, histology, and backscattered elec- tron scanning electron microscopy (BSE SEM) to address this question (Fig. 2 and figs. S5 to S13). Using this combination of methods, we found that elephant predigits initially form as massive, purely cartilaginous rods and that these can become further stiffened through a slow con- version to bone (that is, forming endochondrally) by an unusual ossification mechanism. Histolog- ical examination showed that this initial hyaline cartilage element lacks a preferential orientation of chondrocytes or growth-plate–like stratification (fig. S13). Imaging with BSE SEM and CT in addition to histology revealed that patches of this cartilage calcify and are resorbed and replaced by bone that subsequently models to a foam- or honeycomb-like cancellous (spongy bone) struc- ture. The advancing mineralizing fronts and the thickness of the calcified cartilage layers resem- ble those seen in mature articular cartilage.

Together, our analyses not only show that the cartilaginous predigits are slowly replaced by bone during late ontogeny, but that this bone is unusual in its development [Fig. 2, supporting online material (SOM) text, and figs. S5 to S13]. Ossification typically begins years after other ses- amoids have become well mineralized (for ex- ample, the proximal digital sesamoids, at ~3 to 7 years of age), and it occurs in a large cartilage structure surrounded by a fat pad rather than by tendon or ligament. Such ossification can remain incomplete [in 10 out of 37 (10/37) feet exam- ined] or even uninitiated (11/37 feet) in some adult (~20+ years old) individuals (figs. S4 to S6). This singular mode of ossification is endochondral, ex- tending from several seemingly haphazardly po- sitioned centers within the massive cartilaginous precursor. Furthermore, BSE SEM and CT indi- cate that the resultant cancellous (spongy) bone, unlike others in the appendicular skeleton, does

not seem oriented to match any predominant load- ing direction and lacks compact cortices, which could confergreater longitudinal bending stiffness. This indicates an unusually flexible ossified struc- ture that nevertheless is stiffer than the surrounding fat pad or cartilage, although even cartilaginous enlarged predigits should provide some support.

We used an indirect approach to solve the difficult question of how elephant predigits func- tion. Elephant predigits are deeply embedded in the digital cushions or fat pads of the feet, thus their positions and motions are obscured. The thick keratinized skin of elephant feet prevents ultrasound or x-ray imaging at safe intensities, thus preventing in vivo investigation. We pre- viously speculated that elephant predigits might function as strut-like weight supports, because they grow with strong positive allometry simi- lar to that of the metapodials (16). This function would be expected to involve a static orientation of the predigits during loading. Alternatively, pre- digits might function as dynamic levers (more

like mobile digits) if they reoriented when loaded, rotating about their joint(s). Animals variably em- ploy similar functions with their true digits (17).

We tested these hypotheses by statically loading cadaveric elephant feet ex vivo and CT- scanning them to examine the effects of applied loads on their orientation (11). Predigits behav- ing in a weight-supporting role should maintain a constant orientation, whereas predigits acting as dynamic levers should display joint mobility (movie S2) that reorients them with increasing load. Our reconstructions (Fig. 3) reveal that the prepollex and prehallux act differently when loaded: The prepollex does not move apprecia- bly even though its proximal joint allows some mobility, whereas the prehallux rotates caudo- dorsally. Internal motion contributing to this ro- tation is apparent for the prehallux which, once ossified at least, is consistently split into prox- imal (fixed to the first metatarsal and tarsal) and distal (free to move) segments (evident in 8/8 individuals with well-ossified prehalluces; movie

Fig. 1. Foot anatomy in humans and elephants, with sesamoids shown in white. (Top) Diagram of human manus and pes (for comparison). Dotted lines for the prepollex and prehallux show rough approximations of where these structures would lie in humans, but they are normally absent. These predigits are not to be confused with the paired digital sesamoids, which elephants and humans have more distally in their digits—the so-called “tib- ial sesamoid” in humans is one of these. (Middle and bottom) Elephant foot anatomy in medial view of right feet. The manus is on the left [pre- pollex (dark) and meta- carpal I shown below]; the pes is on the right [prehallux (dark) and me- tatarsal I shown below]. Bottom-row images are from CT scan reconstruc- tions of specimen no. 4 (table S1). See movie S2 for representative mobil- ity of a predigit. Osteo- logical terms are from (25, 26). Labels are as fol- lows: ac, accessorium (pi- siform); ca, calcaneus; D3, third digit; ds, digi- tal sesamoid(s); mc1, metacarpal I; mt, meta- tarsal I; ph, prehallux; pp, prepollex.

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S1). The prehallux thus has a proximal portion that statically transfers load to the tarsus (anal- ogous to the whole prepollex), and a distal, mo- bile, lever-like portion. Such segmentation was not apparent in any of our prepollex specimens, which behaved as simple struts. This difference in prepollex and prehallux mobility and function

may relate to the more upright manus and more horizontal pes bone orientations (Fig. 1). Both types of predigits, however, are particularly well suited to stiffen the highly compliant fat pad against excessive deformation. Furthermore, the predigits’ tight syndesmotic articulations with the carpus and tarsus indicate that they also are

able to transfer loading proximally from the sole of the fat pad to those bones, partly bypassing the digits. Therefore, the enlarged predigits render elephant feet functionally plantigrade while the true digits remain in subunguligrade orientations. Indeed, the predigits may allow elephants to ef- fectively reduce the degrees of freedom in their

Fig. 2. Histology of elephant predigit, from speci- men no. 2 (table S1) prepollex. (A) Toluidine blue histology of bone:cartilage interface [proximal slab 4 (fig. S6); cartilage, dark blue, bone, pale blue, bone marrow space, white; width = 1200 mm]; see also fig. S13. (B) BSE SEM macerated slab 1 (width = 34 mm). The large space in the right central area (see also fig. S9) was occupied by cartilage and shows the endochondral mineralization front [higher magnifi- cation in (C), width = 1204 mm]. (D) BSE SEM of polymethylmethacrylate-embedded slab 0 (width = 28 mm; see also fig. S7) with a pseudocolor look- up table. The lowest backscattering coefficient (top) is level from the monobrominated standard and highest at 255 from the monoiodinated di- methacrylate standard (27); the densest phase is calcified cartilage. (E) Higher-magnification gray image of the calcified cartilage:bone interface (width = 900 mm). Enlarged versions of images (B) to (E) are in figs. S8 and S10 to S12.

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Fig. 3. Passive motion of elephant predigits under loading. Right cadaveric manus (top row) and pes (bottom row) specimens under minimal (left) and maximal (right) loads are shown. In the manus, the prepollex does not move noticeably relative to the vertical, whereas the metacarpal dorsiflexes up to 13° at maximal load. In the pes, the distal segment of the prehallux rotates around the static proximal segment, dorsiflexing up to 17° as the metatarsal dorsiflexes up to 10°. Bones (Fig. 1) are colored to match movies S1, S3, and S4. Predigits are aqua- marine color. Specimen numbers from table S1 are no. 3 (manus) and no. 5 (pes). Labels are as fol- lows: MC3, metacarpal 3; MT3, metatarsal 3; ph, prehallux; pp, prepollex.

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feet, by providing a more passive stabilizing sup- port that reduces need for more active and mas- sive muscular tissues, analogous to the reduction of toes in other ungulate groups (18). Yet the persistence of musculotendinous structures an- chored to these sesamoids [such as the abductor pollicis (9)] indicates some retained ability to control their position or caudolateral motion, so the predigits are not entirely passive structures.

There is a smooth ridge on the caudomedial surface of metacarpal I with which the prepollex articulates, as well as a mobile ball-and-socket– like joint on the distal end of tarsal I and a ridge on the caudomedial side of metatarsal I that both articulate with the prehallux (15). These features, found even in juvenile elephants that lack ossified predigits, are thus osteological correlates of the presence of predigits (Fig. 1) that might be iden- tifiable in fossils. Their presence in any skeletal specimen would corroborate the existence of en- larged predigits (cartilaginous or ossified).

Our survey of the fossil record of the clade Proboscidea revealed some evidence of predigits in extinct forms (11), which also clarifies how elephant foot posture and function evolved. Un- fortunately the most basal proboscideans (such as Barytherium and Numidotherium) lack suffi- ciently well-preserved metapodials (and thus po- tential evidence of predigit articulations) to more

directly test whether they had large predigits. However, their preserved proximal carpal and tarsal elements show that the feet were quite plantigrade, leaving little space for an expanded digital cushion or predigits (Fig. 4, movies S3 and S4, and SOM text). Furthermore, the artic- ulations of more distal foot bones indicate the presence of relatively dorsiflexed and more splayed (abducted) toes; not as adducted as in later Pro- boscidea and consistent with a more amphibious lifestyle. Hence we infer that basal proboscideans, like many of their amphibious or wholly aquatic tethytherian outgroups [Sirenia and Embrithopoda (19)] were more plantigrade than extant elephants, as is ancestral for tetrapods.

We therefore hypothesize that the evolution of more subunguligrade toes in elephants is linked with the expansion of the manual and pedal digital cushions and their supporting predigits. In this scenario, the predigits increasingly adopted the supportive roles that were played by the carpals (e.g., pisiform) and tarsals (e.g., calcaneus) in more plantigrade basal Proboscidea. Representative elephantiform and deinothere taxa along the phy- logeny (Fig. 4) before Elephantidae support this hypothesis (SOM text, figs.S14 to S16, and movies S3 and S4): All well-preserved taxa exhibit smaller proximal carpal/tarsal bones and foot bone articu- lations that are more consistent with increased

dorsiflexion of the toes, and thus a more subunguli- grade toe posture relative to the ancestral condition for Proboscidea. All of these taxa display osteolog- ical correlates for the articulation of predigits in the manus and pes. Thus, we conclude that the pre- digits have served to stiffen the expanded fat pad and maintain a plantigrade-like foot function, trans- ferring loads from the substrate to the carpus/tarsus, since early in elephantiform evolution.

Extant elephants have remarkable feet that combine advantages of plantigrady [such as the potential for damping impacts at heelstrike (20), larger foot surface area and thus moderated pressures (21), large translations of the center of pressure during the stance phase involving pro- nounced heelstrike, dynamic gearing, and toe- off dynamics (17)] with those of digitigrady or subunguligrady [such as reasonable mechanical advantage of the toes to keep supportive tissue stresses at safe levels (22), or even potential ben- efits to metabolic economy from elastic energy storage (23)]. These changes occurred while early elephantiforms attained gigantism (>2000 kg of body mass or shoulder height >2 m) in the Eocene epoch (~40 million years ago, Fig. 4) and occupied a wider range of terrestrial habitats, be- coming less amphibious around the node joining Deinotheriinae and Elephantiformes (Fig. 4). Hence, there is probably a link between the in-

Fig. 4. Evolution of pro- boscidean foot posture. A stratigraphically time- calibrated axis is shown at top, using the phyloge- netic tree from (28–30), with clades Proboscidea, Elephantiformes, and El- ephantoidea labeled at nodes; the Sirenia (sea- cows; manatees and du- gongs) extant outgroup is shown. Manus (on left) and pes (on right) speci- mens are shown in ap- proximate osteologically neutral poses in lateral view (more explanation and images are in the SOM text and figs. S14 to S16). Movies S3 and S4 show three-dimensional foot reconstructions and predigit articular surfaces (where present). A shift from a relatively more plantigrade manus and pes in Numidotherium and Barytherium to more subunguligrade feet in later taxa is evident, es- pecially when articular surfaces are compared. Shoulder heights (top of scapula) for each genus are roughly estimated in parentheses, as a proxy for body size changes. Representative skeletons of Barytherium (top) and Deinotherium (bottom) are shown with approximate relative size differences.

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creasing demands of supporting and moving greater weight on land and the benefits of having more upright toe bones but directing some loads away from the toes with the predigits and fat pad, which resulted in the peculiar compromise that persists in the feet of extant elephants.

The recognition of elephant predigits as en- larged sesamoids that perform digit-like functions fuels inspiration for examining the evolution of foot function, terrestriality, and gigantism in other lineages. Sauropod dinosaurs had expansive foot pads, particularly in their pedes (24); however, no evidence of predigits has been found. Con- sidering that the predigits form on the medial border of the feet, they would tend to be lost if digit I is lost or reduced, as it was in early peris- sodactyls and artiodactyls. This loss might limit foot pad expansion and thereby explain why rhinos and hippos seem to lack predigits [but see (18) for a possible rudimentary pollex in hippos] and have less expanded foot pads than elephants do (8). Regardless, the previously misunderstood and neglected predigits of elephants now deserve recognition as a remarkable case of evolutionary exaptation (4), revealing how elephants evolved their specialized foot form and function.

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Acknowledgments: We thank the staff of the Structure and Motion Laboratory of the Royal Veterinary College for assistance and three anonymous reviewers for constructive criticism. Many individuals assisted with the collection of the cadaveric data; we particularly thank the European-based zoos that provided the specimens and G. Fritsch for CT scans done in Germany. O. Cosar, R. Weller, A. Wilson, and K. Jespers assisted with the ex vivo loading experiments. J. Molnar assisted with Figs. 1 to 4 and the movies. This project was funded by the Biotechnology and Biological Sciences Research Council (BBSRC) (grants BB/C516844/1 and BB/H002782/1 to J.R.H.). Additionally, A.A.P. appreciates funding from Arthritis Research UK and the BBSRC, and A.B. was supported by the Veterinary Advisory Committee of the UK Horserace Betting Levy Board. The data reported in this paper are tabulated in the SOM. The authors declare no conflicts of interest.

Supporting Online Material www.sciencemag.org/cgi/content/full/334/6063/1699/DC1 Materials and Methods SOM Text Figs. S1 to S16 Tables S1 to S3 References (31–41) Movies S1 to S4

20 July 2011; accepted 8 November 2011 10.1126/science.1211437

Global Seabird Response to Forage Fish Depletion—One-Third for the Birds Philippe M. Cury,1* Ian L. Boyd,2* Sylvain Bonhommeau,3 Tycho Anker-Nilssen,4

Robert J. M. Crawford,5 Robert W. Furness,6 James A. Mills,7 Eugene J. Murphy,8

Henrik Österblom,9 Michelle Paleczny,10 John F. Piatt,11 Jean-Paul Roux,12,13

Lynne Shannon,14 William J. Sydeman15

Determining the form of key predator-prey relationships is critical for understanding marine ecosystem dynamics. Using a comprehensive global database, we quantified the effect of fluctuations in food abundance on seabird breeding success. We identified a threshold in prey (fish and krill, termed “forage fish”) abundance below which seabirds experience consistently reduced and more variable productivity. This response was common to all seven ecosystems and 14 bird species examined within the Atlantic, Pacific, and Southern Oceans. The threshold approximated one-third of the maximum prey biomass observed in long-term studies. This provides an indicator of the minimal forage fish biomass needed to sustain seabird productivity over the long term.

P ublic and scientific appreciation for the role of top predators in marine ecosystems has grown considerably, yet many upper

trophic level (UTL) species, including seabirds, marine mammals, and large predatory fish, re- main depleted owing to human activities (1–4). Fisheries impacts include direct mortality of ex- ploited species and the more subtle effects of altering trophic pathways and the functioning of marine ecosystems (5). Specifically, fisheries for lower trophic level (LTL) species, primarily small

coastal pelagic fish (e.g., anchovies and sar- dines), euphausiid crustaceans (krill), and squid (hereafter referred to as “forage fish”), threaten the future sustainability of UTL predators in marine ecosystems (6, 7). An increasing global demand for protein and marine oils contributes pressure to catch more LTL species (8). Thus, fisheries for LTL species are likely to increase even though the consequences of such activity remain largely unknown at the ecosystem level. It remains challenging, however, to assess fishing

impacts on food webs because numerical re- lationships between predators and prey are often unknown, even for commercially valuable fish (9, 10). Ecosystem models and ecosystem-based fisheries management, for which maintaining

1Institut de Recherche pour le Développement, UMR EME-212, Centre de Recherche Halieutique Méditerranéenne et Tropi- cale, Avenue Jean Monnet, BP 171, 34203 Sète Cedex, France. 2Scottish Oceans Institute, University of St Andrews, St Andrews KY16 8LB, UK. 3Ifremer, UMR EME 212, Centre de Recherche HalieutiqueMéditerranéenneetTropicale,AvenueJeanMonnet, BP 171, 34203 Sète Cedex, France. 4Norwegian Institute for Nature Research, Post Office Box 5685 Sluppen, NO-7485 Trondheim, Norway. 5Branch Oceans and Coasts, Department of Environmental Affairs, Private Bag X2, Rogge Bay 8012, South Africa. 6College of Medical, Veterinary and Life Sciences, Uni- versity of Glasgow, Glasgow G12 8QQ, UK. 710527 A Skyline Drive, Corning, NY 14830, USA. 8British Antarctic Survey, High Cross, Madingley Road, Cambridge CB3 0ET, UK. 9Baltic Nest Institute, Stockholm Resilience Centre, Stockholm University, SE-106 91 Stockholm, Sweden. 10Fisheries Centre, Aquatic Ecosystems Research Laboratory (AERL), 2202 Main Mall, The University of British Columbia, Vancouver, BC, Canada V6T 1Z4. 11U.S. Geological Survey, Alaska Science Center, 4210 Uni- versity Drive, Anchorage, AK 99508, USA. 12Ecosystem Analysis Section, Ministry of Fisheries and Marine Resources, Lüderitz Marine Research, Post Office Box 394, Lüderitz, Namibia. 13Animal Demography Unit, Zoology Department, University of Cape Town, Private Bag X3, Rondebosch, Cape Town 7701, South Africa. 14Marine Research Institute and Zoology Depart- ment, University of Cape Town, Private Bag X3, Rondebosch, Cape Town 7701, South Africa. 15Farallon Institute for Advanced Ecosystem Research, Post Office Box 750756 Petaluma, CA 94952, USA.

*To whom correspondence should be addressed. E-mail: [email protected] (P.M.C.); [email protected] (I.L.B.)

www.sciencemag.org SCIENCE VOL 334 23 DECEMBER 2011 1703

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