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This reprint is provided for personal and noncommercial use. For any other use, please send a request to Permissions, American Scientist, P.O. Box 13975, Research Triangle Park, NC, 27709, U.S.A., or by electronic mail to [email protected]. ©Sigma Xi, The Scientific Research Society and other rightsholders FEATURE ARTICLE

Modern Lessons from Ancient Food Webs

From the Cambrian Burgess Shale to ancient Egypt, food webs share surprising structural attributes. When redundancy is lost, the threat of extinction grows.

Justin D. Yeakel and Jennifer A. Dunne

bout 10,000 years ago, one patterns of feeding interactions be- systems is more complete when we could have mistaken the tween and among species (food web unite the detailed but temporally lim- Egyptian landscape for that structure) and changes in species’ ited knowledge of modern ecological of East Africa today. Instead abundance over time (dynamics) of systems with the wealth of informa- Aof vast arid deserts, the region north of the Egyptian mammal community is tion obtained from historical and pale- Aswan held enough annual precipita- providing insight into how this ecosys- ontological contexts. tion to support large herbivores that tem unraveled in the face of both cli- Recent investigations into the struc- are strongly tied to standing bodies of matic and human-induced pressures. ture and dynamics of past and contem- water, including zebra, elephant, and But the observed community collapse porary food webs has shown that there rhinoceros. Lions, wild dogs, giraffes, in Egypt is just a small piece of a much is a certain fixedness in the patterns and wildebeest filled out the savanna- larger story that describes the rise and of species interactions, independent woodland landscape, while the earliest fall of animal communities over the of species identity, habitat, and time. pyramids were still thousands of years last 540 million years of multicellular However, this fixed structure appears in the future. This was Egypt during life on Earth. to be sensitive to external disturbances, the African Humid Period, which end- As with the analysis of ancient in particular large-scale events such as ed roughly 5,500 years ago, when the Egyptian ecosystems, a central goal in mass extinctions. The structural fea- moisture supplied to equatorial Africa ecology is to understand how animal tures common to food webs, as well by seasonal monsoons declined, result- and plant communities arise, change, as their sensitivity to disturbances, are ing in an increasingly arid climate. and respond to disturbances both large relevant to our ability to predict (and It was just after the African Humid and small. To that end, ecologists have perhaps engineer) the fate of modern Period that urban centers began to de- adopted new tools designed to inves- biological systems. Integrating con- velop around the Nile Valley. As hu- tigate ecological networks and help us temporary ecology with observations mans shifted to agriculture and popu- uncover and understand past extinc- of the past will provide key insights lation densities grew, the local animal tions and their community-level con- into the future risks and uncertainties community became increasingly mar- sequences in the hopes of predicting facing the multitude of species with ginalized. The cumulative evidence of those in the future. To do so, we com- which we share the planet. mammalian species present in Egypt pare reconstructions of past ecological before the end of the African Humid networks, such as food webs, to mod- Food Webs in Deep Time Period, taking into account paleonto- ern biological communities in an effort The behaviors of all evolutionarily suc- logical and archeological observations, to identify similar drivers of change. cessful organisms are constrained by reveals 37 larger-bodied species occu- Analysis of the structure and func- two major dictates: They must pass pying the region. Of those 37, only 8 tion of modern and paleontological down their genetic material, and they remain today. This massive loss of bio- ecosystems falls within the bounds must acquire the necessary energy to do diversity likely resulted from a combi- of complex systems science, a bur- so. Plants and other organisms that can nation of factors: habitat loss, hunting, geoning suite of research topics that make their own food generate their own and local and regional climate change. unite many aspects of mathematical, energy; herbivores, carnivores, and om- Reconstructing how extinctions physical, and biological sciences. As nivores must find, capture, and consume throughout the Holocene affected the researchers at the Santa Fe Institute their food to acquire energy. In a commu- in New Mexico—a not-for-profit or- nity of many species, the sum total of the Justin D. Yeakel is an Omidyar Postdoctoral Fellow at ganization centered around the study patterns of interactions that characterize the Santa Fe Institute. Jennifer A. Dunne is a profes- of complex adaptive systems—we these processes can appear to be a chaot- sor and the Vice President for Science at the Santa Fe think that our understanding of the ic tangle. In fact, they comprise a highly Institute. E-mail for Dr. Yeakel: [email protected]. underlying organization of natural organized network of who eats whom.

188 American Scientist, Volume 103 © 2015 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. Griffith Institute/University of Oxford Determining how these communi- Depictions of animals, such as this hunting scene from one side of King Tutankhamun’s Painted ties function requires not only knowing Box, built more than 3,000 years ago, document the mammal community of ancient Egypt over which species are present and when, time. Piecing together ancient food webs can help us understand their fundamental properties. but how they interact. In a relatively recent development, ecological research- power grids, research on ecological counts of feeding links for each con- ers are now borrowing tools from networks such as food webs shows sumer are normalized (divided by the graph theory and nonlinear dynamics, that they have nonrandom structure. average number of links per species in analyzing the structure of ecological This property implies that there are its food web). communities as networks, with nodes underlying forces that constrain inter- The remarkable similarity of the representing species or groups of sim- actions between species, much as there structure of modern food webs gives ilar species and links representing a are underlying—though different— rise to a tantalizing question: Have type of interaction. For example, food forces constraining the formation food webs always been this way? In webs are ecological networks where of friendships in social networks or other words, is the fundamental struc- links represent a flow of biomass be- transmission lines in power grids. ture of food webs fixed? If food webs tween two species, and the patterns of More surprising, food webs, indepen- have an underlying structure that is these feeding interactions determine dent of locality, habitat, and species maintained across different ecosys- the structure of the community. composition, appear to share a num- tems over evolutionary time, there This nonrandom organization is in ber of regularities in their organiza- may be fundamental rules driving part responsible for the dynamics of tion. For instance, the distribution of ecological interactions independent of the system: how long the system is ex- feeding links across species (the de- species, habitat, or community. If some pected to persist, whether it is sensitive gree distribution, which characterizes underlying mechanism guiding com- to external disturbances, and to what the relative abundance of specialist munity structure exists, they might re- extent it can recover after a disturbance or generalist feeders) is similar across spond similarly to large perturbations. has ended. In addition to a large and food webs, such that most species are In this case, such knowledge could growing body of work on contempo- quite specialized and a very few are directly inform management of con- rary ecological networks, uncovering highly general feeders. temporary ecosystems in the wake of the structure of paleontological or his- Because food-web structure is sys- current or future perturbations. torical communities provides a means tematically sensitive to the numbers To address these questions, one to understand how they evolve and of species and links represented in the must look into the fossil record, and change over long periods of time, and system, when this scale dependence is the Cambrian-era Burgess Shale fauna to gauge how they respond to known accounted for, the remarkable regular- is about as far back in time as preser- large-scale changes in the environment. ity of the degree distribution is uncov- vation allows for ecosystem-level anal- Much like other kinds of real-world ered. In this case, the general pattern ysis. The Burgess Shale was formed networks including social groups and across food webs only emerges when more than a half a billion years ago, www.americanscientist.org © 2015 Sigma Xi, The Scientific Research Society. Reproduction 2015 May–June 189 with permission only. Contact [email protected]. Great Pyramid constructed

aridi cation urban event ends 2nd 3rd expansion African Humid aridi cation aridi cation in the Period event event Mediterranean

African Humid Period

11,000 10,000 9,000 8,000 7,000 6,000 5,000 4,000 3,000 2,000 1,000 0 thousands of years ago

millions of years ago

Mass Mass Mass Extinction Extinction Extinction

Cambrian explosion Permian Cretaceous Eocene

600 550 500 450 400 350 300 250 200 150 100 50 0 millions of years ago millions of years ago when a muddy embankment col- lucigenia. However, it turns out that in communities emerged early in the lapsed on a shallow sea community there are many ways to infer feeding history of multicellular life. Second, it that now lies interred in the Canadian from the Burgess fossils, for example implies that the structure of food webs Rockies. The species in this ecosystem from fossilized gut contents, from is largely independent of the identity were shelled or plated invertebrates the matching of mouthparts to bite and history of their component spe- that crawled and swam along the marks, and from constraints of body cies. Third, it implies that the core shores of the Panthallasic Ocean, and size. Many of the inferred feeding food-web structure of ecological sys- have been a subject of intense study links can be assigned with relative- tems is—in the long run—relatively for much of the 20th century. Stephen ly low uncertainty, and analyses of resilient to large-scale perturbations to Jay Gould remarked of the fossils in the resulting food web can account the biosphere. his book on the Burgess Shale, Wonder- for how sensitive the assessment of ful Life: “They are grubby little crea- structure is to whether low-certainty Predicting Extinctions tures of a sea floor 530 million years links are included or excluded. To what extent global perturbations old, but we greet them with awe be- Although many Burgess lineages disrupt ecological communities, and cause they are the Old Ones, and they were evolutionary dead ends, and taxa how these systems contract or reas- are trying to tell us something.” giving rise to modern lineages looked semble after a perturbation, are topics The Burgess Shale fossils, which are different from their descendants, the that have important implications for remarkably well preserved, give a sur- patterns of feeding interactions are modern ecosystems. For example, the prising amount of evidence about spe- surprisingly similar to those of today. end-Permian mass extinction (251 mil- cies’ morphologies, evolutionary rela- For example, food webs for both the lion years ago) marks the largest die- tionships, and ecological roles. As such, Burgess Shale and an earlier Cambrian off in Earth’s history, resulting in the this ancient assemblage provides an ex- community in China (the Chengjiang extinction of 70 percent of terrestrial citing opportunity to test the notion of Shale) had normalized degree distri- vertebrates and 96 percent of marine fixedness in the structure of food webs. butions indistinguishable from mod- species. The early Triassic communi- Reconstructing the feeding inter- ern ecosystems (see figure below). ties that emerged immediately after actions of the Burgess Shale is no The implications of this structural this extinction differed substantially easy task, particularly with species durability are profound. First, it sug- from those in the Permian, having a whose strange morphologies inspire gests that the forces shaping the over- greater diversity of amphibian versus names such as Anomalocaris and Hal- all structure of species interactions amniote species.

1.00

(520 Ma) Cambrian food webs (505 Ma)

0.10 modern food webs from eight Food webs, such as the one from the Cambrian Burgess Shale shown different above, are made up of nodes (spheres, representing species or groups sites of species) and links (green lines, representing who eats whom). Yellow spheres show top predators, whereas red spheres represent primary producers and decomposers. Food webs across geological time share

cumulative probability distribution cumulative remarkable structural similarities. The probability distribution at left shows the prevalence of the number of links across the nodes in a network, normalized by the size of the network. The graph shows that all links nodes with a large number of feeding links (those toward the right side of the x-axis) are rare. The shape of this curve portrays deep informa- 0.01 tion about a network’s structure, and the fact that all of these food webs 0.01 0.10 1.00 10.0 across geological time have similar cumulative link distributions is normalized number of food-web links incredible. Figures adapted from J. A. Dunne, et al., 2008.

aridi cation urban event ends 2nd 3rd expansion African Humid aridi cation aridi cation in the Period event event Mediterranean

African Humid Period

11,000 10,000 9,000 8,000 7,000 6,000 5,000 4,000 3,000 2,000 1,000 0 thousands of years ago

Mass extinctions at the end of the Permian and Cretaceous, respectively (left), and the aridi- Mass Mass Mass fications in ancient Egypt (below), disrupted Extinction Extinction Extinction food webs. These networks are more susceptible to extinction cascades after such large-scale events. After the mass extinctions, the food webs eventually recovered over millions of Cambrian explosion Permian Cretaceous Eocene years—with new sets of species. Across time, food-web structure appears to be predictable. 600 550 500 450 400 350 300 250 200 150 100 50 0 millions of years ago millions of years ago

Great Pyramid thousands of years ago constructed

aridi cation urban event ends 2nd 3rd expansion African Humid aridi cation aridi cation in the Period event event Mediterranean

African Humid Period

11,000 10,000 9,000 8,000 7,000 6,000 5,000 4,000 3,000 2,000 1,000 0 thousands of years ago A second mass extinction that fa- proportion of species that are likely to posed much greater risks to surviving mously occurred 66 million years ago lose all of their food sources following species. The structure of food webs fol- (the Cretaceous-Paleogene extinction) a simulated disturbance that results lowing large disturbances appears to was likely initiated by an asteroid im- in one or more primary extinctions. increase the likelihood of additional pact and resulted in the disappearance Food webs with a lower proportion of extinctions, yet food web structure of nonavian dinosaurs, thus setting secondary extinctions based on these appears remarkably stable over large the stage for mammalian diversifica- simulated disturbances are generally periods of time. Somehow biological Mass Mass tion. Prior to this extinction event, dur- expectedMass to be more robust than those communities must recover these struc- Extinction Extinction ing the end-Cretaceous, was a large withExtinction a higher proportion, because they tural attributes after disruptions—but shift in dinosaur species composition, are expected to be more resistant to ex- how, and how quickly? which may have left these systems tinction cascades. Events after the Cretaceous- Cambrian explosion Permian vulnerable to the asteroid impact.Cretaceous Re- SimulationsEocene of perturbations initiat- Paleogene extinction offer clues. The cent analyses led by Peter Roopnarine ed at the base of the community strad- disappearance of nonavian dinosaurs of the California Academy of Sciences dling the end-Permian demonstrated made room for the diversification of 600 550 500 450 400 350 300 250 200 150 100 50 0 and Jonathan Mitchell of University that robustness was lower in the post- mammals, many species of which in- millions of years ago of Chicago, respectively, millionshave shown of years agoperturbation Triassic versus the pre- creased in body size, perhaps filling that both post-perturbation communi- perturbation Permian. Similarly, the similar ecological roles as their extinct ties (the Triassic following the Perm- restructuring of end-Cretaceous com- saurian cousins. The Eocene (56 to 33.9 ian, and the end-Cretaceous) exhibited munities led to a decline in robustness million years ago) marked a pinnacle shifts in feeding interactions between immediately before the Cretaceous- of mammalian evolution, witnessing surviving species that resulted in a re- Paleogene extinction event, potentially the diversification of hooved mam- structured food web. creating the conditions for the mass mals, carnivores, and early primates, Such changes to food-web structure extinction that followed. Although among others. The Eocene mamma- offer a way to study and measure al- extreme perturbations tend to lead lian community evidently was a di- tered ecosystem functioning, which can to subsequent domino-effect extinc- rect recipient of the ecological space be estimated by calculating community tions as the base of the food web is cleared by the events occurring before robustness, the resistance of a system eroded, the patterns of interactions and during the Cretaceous–Paleogene to change in the face of an imposed in pre-perturbation communities ap- extinction, but did this leave a lasting perturbation. Communities that absorb pear to be more resistant to the effects imprint on food-web structure? perturbations and remain relatively un- of smaller disruptions. This observa- Recent analysis of food webs for a altered are considered robust, whereas tion suggests that ecosystems in the 48-million-year-old small maar lake those that are reactive and prone to Permian and mid-Cretaceous were and the surrounding paratropical for- reorganization or contraction are not. more robust, whereas the structural est (now located in Germany) indicate Accordingly, if the structure of the com- organization of early Triassic and late that—in the long run—it did not. The munity is known, and given some basic Cretaceous communities was more food-web structure of these Messel assumptions regarding the dynamics easily unraveled. These restructured Shale ecosystems (comprising 700 lake that regulate how populations change communities were likely fragile, such and forest taxa, thereby exceeding the over time, one can then determine the that successive environmental changes resolution of extant food web data sets)

www.americanscientist.org © 2015 Sigma Xi, The Scientific Research Society. Reproduction 2015 May–June 191 with permission only. Contact [email protected]. revealed unambiguous similarities with The Egyptian modern ecosystems. This finding suggests that the structuring of food-web Food Web relationships observed within modern animal communities—also evident in the Cambrian—unfolded at least 18 million years after the asteroid impact. Despite a sensitivity to disturbance, the structural features common to both modern and paleontological food webs have survived five major and many minor extinction events. This structural reemergence points to con- sistent ecological mechanisms constraining interactions between species, despite the major evolutionary, environmental, and climatic transitions 11,760 before present distinguishing the last half-billion years of Earth’s history.

Humans in Ancient Food Webs There is increasing convincing evidence that we are currently nearing the brink of a sixth mass extinction, resulting from human impacts related to climate change, land-use changes, and other anthropogenic drivers of extinctions. If it is assumed that all threat- ened species go extinct within a century, and that such an extinction rate is maintained, it is expected that 75 percent of species will become extinct in about 250 to 500 years. Understanding the effects of large-scale disturbances on the structure and functioning of ecosystems thus requires higher resolution observations of biological com- 4,640 before present munities over more recent timescales. In this case, we shift our focus from the fossil record to the historical record. During the past 50,000 years, a com- bination of natural climatological and human-induced changes have shaped animal communities. The latter have become particularly significant in the last 15,000 years, as populations have migrated into unpeopled continents and islands, invading existing food webs. In some cases, hunter-gatherers may have migrated into ecosystems without significantly altering long- term food-web organization, as sug- gested by research from the eastern Aleutian Islands in the North Pacific. In Beringia—a region including the Yukon, Alaska, northeastern Siberia, today and the landmass now located on the seafloor of the Bering Strait—humans The mammalian food web of Egypt lost its redundancy as the climate became more arid and may have moved into ecosystems that human population densities increased. Most notably midsized herbivores—such as gazelles had already been significantly reorga- that link to the most carnivores—declined. Mammal species remaining in the food web nized by the Last Glacial Maximum, today (bottom panel) are much more susceptible to disturbance than those in the rich as- a large climatic perturbation that oc- semblage of the African Humid Period (top). Some species are lumped with congeners here. curred near the end of the Late Pleisto-

192 American Scientist, Volume 103 © 2015 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. cene. In other cases, humans a local context afterward. The may have played a strong dama deer, thought to have role in restructuring the eco- migrated across the Isthmus system, evidenced by, for in- of Suez during the Pleisto- stance, changing interactions cene, is found in contempora- between seed dispersers and nious fossil deposits in Egypt seed-bearing plants in the Pan- and is depicted on mace han- tanal, Brazil. Where humans dles and in hunting scenes settled into dense and expand- until the 18th Dynasty (circa ing agricultural societies, the 3,270 years ago). Carnivores, potential for effects on food- including leopards, cheetah, web structure, robustness, and wild dogs, spotted hyenas, functioning were high. and possibly two subspecies Ancient Egypt is one of the of lions, were ancient inhabit- most extreme transitions to ants of Egypt, but today are dense urban settlements in the The Eocene Messel Shale food webs, such as this one reconstructed all locally extinct, having dis- from fossils in a small maar lake, show unequivocal similarities historical period and is unusu- appeared at different times with modern ecosystems. Species are arranged along the vertical ally well documented, mak- axis from primary producers (bottom) to higher order consumers during the past 6,000 years. ing it a powerful case study of (top), with color indicating types of organisms: vertebrates (or- The rise of urban societies in such effects, especially during ange), invertebrates (yellow), bacteria and fungi (blue), and plants Egypt occurred in an environ- a period of concurrent climatic and phytoplankton (green). From J. A. Dunne, et al., 2014. ment with a rich assemblage change. The region around of mammalian species. Over the Nile floodplain primarily the same time frame, there supported nomadic pastoralists until Egyptian data. In the body of artistic were three well-documented aridi- the end of the African Humid Period work, depictions of species disappear fication events, each occurring over a 5,500 years ago. Permanent agricul- at different times, likely as a conse- relatively short period, that have been tural societies emerged soon after, per- quence of local extirpation. Combin- associated with major political disrup- haps in response to a landscape that ing those data with evidence of species tions and famines: The first, about 5,050 was becoming increasingly arid. It was occupation in the fossil record permits years ago, marked the beginning of the during the latter half of the Holocene a detailed reconstruction of how the Egyptian Pharaonic state; the second, (5,000 to 6,000 years ago), as the density community composition changed. circa 4,140 years before present, was of human populations increased and For example, the African elephant linked to the end of the Old Kingdom; the landscape became dominated by is present in early Holocene fossil de- and the third, about 3,035 years ago, desert-adapted flora, the historical ani- posits and is even depicted in rock marked the end of the New Kingdom mal community—comprising 37 larger- engravings credited to Predynastic no- as well as widespread famine in Egypt bodied mammals—was diminished to mads, but it is not found or depicted in and Syria. The expansion of agricultural its current state of 8 species. settlements and human den- Unlike the extinction sities in Egypt and a general events of the deep past, the shift toward aridity—itself collapse of the Egyptian marked by three significant animal community was climatic pulses—are well witnessed by settled hu- suited for examining how man populations, with ar- the structure and dynamics tisans who recorded what of animal communities were they saw in rock, stone tab- influenced by the cumulative lets, ivory knives, and tomb effects of these events. walls. Although artistic re- cordings of animals served Dynamics of Extinction many purposes—from re- In the absence of highly re- ligious iconography to fan- solved and comprehensive ciful decorations—many food-web data, one simple depictions are of animals in way to characterize the ecological contexts. The in- structure of a community is credible temporal resolution to compare the ratio of pred- of these historical observa- ator to prey species. This tions offers an unprecedent- property has been shown to ed account of an animal be relatively stable for long community declining in re- Ashmolean Museum, University of Oxford periods of time in the ma- sponse to human influences This siltstone ceremonial palette excavated from the ancient Upper Egypt rine paleontological record, and a changing climate. city of Hierakonpolis is about 5,150 years old and shows predator-prey with intermittent shifts to Researchers rarely interactions in Egypt at that time. Framed by two wild dogs clasping new values. On the much glimpse transitional states in paws, ostrich, hartebeest, wildebeest, ibex, oryx, and giraffe are depicted shorter timescale considered nature as they are seen in the (as are several fictitious animals such as serpent-necked panthers). here, the ratio of predators to www.americanscientist.org © 2015 Sigma Xi, The Scientific Research Society. Reproduction 2015 May–June 193 with permission only. Contact [email protected]. 100 100 bary sheep, and several species of gazelle, among others. Of those species,

80 80 h u m only four remain today, some of which percent)

( (such as the rhim gazelle) are on the ( a n

mammals m e

60 60 i l o n s verge of extinction. Indeed, simulations birds p o u l a t reptiles of extinctions of the remaining herbi-

40 fish 40 ) vores predict a much larger impact on i o n a b u n d c invertebrates stability than the extinction of any one e

i v 20 plants 20 species historically. What was once a re- humans dundant guild of herbivores has today r e l a t 0 0 been reduced to a few species, the loss 102,015 8,015 2,915 2,515 2,015 1,415 515 215 115 65 15 time of which has a heightened influence on r l t n n l l (before n e a e d d r r a a the stability of the animal community. a r r k io io e e b m e u r r r d d o b present) u th lt a e e o o l lo h u m p p g g As paleobiologists examine an in- e ga ic l l l m m y e - r a a a y e rl t pr r c ic v rl t cultural period te ag s ie la ea la creasing number of food webs before n lo s ea a d hu cl me and after game-changing perturbations, we find commonalities. Similar The food webs of the Adriatic Sea became less diverse, less robust, and more unstable as hu- to analyses of the early Triassic and man densities increased, especially after the rise of the Roman Empire a little over 2,000 years late-Cretaceous post-perturbation food ago. Adapted from H. K. Lotze, et al., 2010. webs, the mammalian community in Egypt appears to have become fragile prey in the Egyptian community clear- ing the height of mammalian species after the trials of the Holocene. The ly shifted. It first increased (relatively richness in Egypt, the food web was loss of a few key species today may more herbivores went locally extinct) highly stable, meaning that the system have a much larger effect on the com- from the end of the Pleistocene until ap- was generally robust to perturbations. munity than at any time in the recent proximately 3,035 years before present, Throughout the Holocene, as the com- past. Changes to community function- and then decreased until 150 years ago munity faced a growing number of ing and dynamics in response to in- (relativelya more carnivores went locally extinctions that altered its size, com- creasing human pressures can be seen extinct),100 and has since increased. position, and patterns of interaction,100 in other impacted ecosystems as well, These shifts are too dramatic to be its dynamic stability declined steadily revealing that anthropogenic distur- h u m e explained80 by random extinctions, in- until a precipitous drop over80 the last bances can alter food webs with last- ( a n c a n

dicating that theremam mwereals different pres- 150 years. This change in stabilitym was ing consequences. i l o n s sures on carnivores and herbivores over insensitive to variability in food p o u l a t web The Adriatic Sea, 1,200 miles north- a b u n d time. Three of the four largest shifts in interactions and to potential error in west of the Nile Valley, is one of the ) e

i v the predator-prey ratio coincide with the timing of extinctions. more productive basins in the Medi- i o n the notable aridification pulses at 5,050, The picture that emerges is straight- terranean. As in Egypt, human pop- r e l a t 4,140, and 3,035 years before present, forward: As the animal community ulations have been present along the although it is not yet clear what caused in Egypt suffered accumulating ex- shores of the Adriatic for nearly 100,000 the differential extinctions. tinctions (due to climate change, hu- years, and urban centers developed Earlier, we identified robustness as an man influences, or both), its ability about 2,700 years ago. An abundance of important property of network dynam- to absorb external impacts eroded— paleontological and archeological sites ics, measured by imposing an extinc- particularly in the last 150 years— in the region, as well as an incredible tion on a community and quantifying leaving behind a fragile ecosystem that array of historical records pertaining the ensuing effects. We now rephrase is a shadow of its historical state. to local natural history, permits recon- this general idea in terms of assessing Although the ultimate causes of the struction of both the occurrence and the effects of applying a small perturba- Egyptian extinctions cannot be deter- approximate abundances of species in- tion to the sizes of populations within a mined based on their observed trajec- habiting marine and estuarine habitats community and assessing the resulting tories, the cause of the decline in stabil- throughout the Late Pleistocene and effects, rather than simulating the loss of ity is more apparent: The system lost Early Holocene in the Adriatic. any particular species as a whole. its redundancy. Food web interactions Even more so than in Egypt, the If the system returns to its prior among larger-bodied mammals are, to cumulative evidence of species abun- state after a simulated perturbation, it a large extent, governed by body-size dance in the Adriatic paints an alarm- is considered dynamically stable, and if limitations: Smaller predators gener- ing picture of human impacts on re- it does not, it is considered dynamically ally consume smaller prey, whereas gional populations. Although humans unstable. Dynamically stable communi- larger predators can consume a larger have hunted and fished for resources ties are more likely to persist because range of prey body sizes. Accordingly, in the Adriatic for tens of thousands of they are assumed to be less reactive to medium-size animals such as gazelle years, there is no evidence to suggest changes in population size levied by are vital components of a functioning human-induced depletion of natural external disturbances. food web, because they form the prey resources until the beginning of the Quantifying dynamic stability of base of the system. Roman Empire. At that time, species’ the Egyptian community over time re- In Egypt during the African Humid abundances declined precipitously, vealed a surprising pattern. At the end Period, such animals were diverse and then recovered, and then fell again of the Pleistocene, a period represent- included gerenuk, sitatunga, ibex, Bar- during and after the Middle Ages.

194 American Scientist, Volume 103 © 2015 Sigma Xi, The Scientific Research Society. Reproduction with permission only. Contact [email protected]. Although analyses of the Egyptian as there is life. However, they will cer- The ability to predict which species and Adriatic systems examined dif- tainly change, and it is evident that our or which communities are most suscep- ferent food webs, some similarities expanding human reach will continue tible to current and future disturbances emerge. First, both suffered from sim- to introduce new challenges. From a lies at the intersection of ecology and plification of the food web. In Egypt, perspective of self-preservation, biologi- conservation, though the answers are this simplification was dramatic, re- cal diversity is the raw material from elusive and whether such an under- sulting in the local extinction of spe- which agriculture, medicine, and all standing is possible is still an open cies. In the Adriatic Basin, although natural resources—including the air that question. Despite this lack of surety, few species were completely extirpat- we breathe—derive. Maintaining intact what is clear is that incorporating les- ed, the abundances of many animals communities of interacting species har- sons from the past is of vital impor- declined drastically—the majority be- bors this diversity, and is thus a require- tance if we are to maintain the current ing species near the top of the food ment for the survival of human societ- diversity of the natural world in the web. These changes can be directly ies. So, the question is not whether the face of an uncertain future. linked to overexploitation by human bridge will fail, but whether the bridge populations. Hence, the Adriatic food goes anywhere we would like to go. Bibliography web suffered a decline in connectance, Barnosky, A. D., et al. 2011. Has the Earth’s meaning that the average number of sixth mass extinction already arrived? feeding interactions per species de- The loss of a few Nature 471:51–57. clined over time. This, in turn, led to Dunne, J. A. , C. C. Labandeira, and R. J. Willia- ms. 2014. Highly resolved early Eocene food a reduction in robustness as defined key species today webs show development of modern trophic by the percentage of secondary extinc- structure after the end-Cretaceous extinction. tions following an initial perturbation. Proceedings of the Royal Society B 281:20133280. The message seems clear: The na- may have a much Dunne, J. A., R. J. Williams, N. D. Martinez, R. ture of human-induced impacts on A. Wood, and D. H. Erwin. 2008. Compi- lation and network analyses of Cambrian animal communities is qualitatively larger effect on the food webs. PLoS Biology 6:e102. different today than in the distant past, Lotze, H. K., M. Coll, and J. A. Dunne. 2010. likely due to the efficiency with which community than at Historical changes in marine resources, large human populations extract re- food-web structure and ecosystem func- sources from the environment, as well tioning in the Adriatic Sea, Mediterranean. as the degraded condition of contem- any time in the past. Ecosystems 14:198–222. porary animal communities compared Maschner, H. D. G., et al. 2009. An introduction to the biocomplexity of Sanak Island, Western to their historical state. We must take From the invertebrate-dominated Gulf of Alaska. Pacific Science 63:673–709. these differences into consideration, Cambrian-era Burgess Shale, to the di- Mitchell, J. S., P. D. Roopnarine, and K. D. An- particularly if we hope to develop a verse mammalian faunas of the Eocene, gielczyk. 2012. Late Cretaceous restructur- framework for predicting how com- to the desert-adapted communities of ing of terrestrial communities facilitated the munities will change in the future. Egypt following the African Humid end-Cretaceous mass extinction in North America. Proceedings of the National Academy Period, there is an underlying thread of Sciences of the U.S.A. 109:18857–18861. A Bridge to Somewhere that unites the patterns of interactions Pires, M., et al. 2014. Reconstructing past eco- A recent survey of bridges in the United between species and their responses logical networks: the reconfiguration of States revealed that 3 percent (or about to disturbance, spanning half a billion seed-dispersal interactions after megafau- 18,000) were deemed fracture critical, years of complex life on Earth. This nal extinction. Oecologia 175:1247–1256. meaning that the failure of a single startling observation not only suggests Roopnarine, P., K. Angielczyk, S. Wang, and R. component could lead to failure of the that there exist fundamental rules de- Hertog. 2007. Trophic network models ex- plain instability of Early Triassic terrestrial entire structure. As with a bridge, the termining how biological communities communities. Proceedings of the Royal Society stability of a food web is determined by organize, but that disruptions to these B 274:2077–2086. the presence and functioning of its com- systems from external events such as Yeakel, J. D., P. R. Guimarães Jr, H. Bocherens, ponent parts. As bridges may collapse climate change may be predictable. and P. L. Koch. 2013. The impact of climate when enough components fail, large Understanding the similarities that change on the structure of Pleistocene food webs across the mammoth steppe. Proceedings perturbations appear to lower the ro- unite modern and ancient food webs of the Royal Society B 280:20130239. bustness of food webs and may require is an ongoing area of intense research, Yeakel, J. D., et al. 2014. Collapse of an ecologi- evolutionary time to recover, whereas and stands to illuminate the principles cal network in Ancient Egypt. Proceedings of accumulating extinctions appear to in- that dictate how communities both as- the National Academy of Sciences of the U.S.A. crease the likelihood of dynamic insta- semble and unravel. Such knowledge 111:14472–14477. bility. However, the comparison of food may also aid conservation efforts by webs with bridges is not a perfect one. enabling identification of species that A bridge that fails ceases to be a bridge; might have an unexpectedly large in- a food web that is unstable remains a fluence on ecosystem function. If such For relevant Web links, consult this food web, though one that is less di- a predictive understanding of commu- issue of American Scientist Online: verse than its ancestral state. nity dynamics is discovered and acted http://www.americanscientist.org/ The imperfection of the bridge anal- upon, we might avoid the potentially issues/id.114/past.aspx ogy points to an important ecological multimillion-year timescales generally truism: Biological communities are not associated with the recovery of food fracture critical—they will exist as long webs in the fossil record. www.americanscientist.org © 2015 Sigma Xi, The Scientific Research Society. Reproduction 2015 May–June 195 with permission only. Contact [email protected].