Geerat J. Vermeij

Approaching a state shift in Earth’s biosphere

Localized ecological systems are known to shift abruptly and irreversibly from one state to another when they are forced across critical thresholds. Here we review evidence that the global ecosystem as a whole can react in the same way and is approaching a planetary-scale critical transition as a result of human influence. The plausibility of a planetary-scale ‘tipping point’ highlights the need to improve biological forecasting by detecting early warning signs of critical transitions on global as well as local scales, and by detecting feedbacks that promote such transitions. It is also necessary to address root causes of how humans are forcing biological changes.

The Mesozoic marine revolution: evidence from snails, predators and grazers

Tertiary and Recent marine gastropods include in their ranks a complement of mechanically sturdy forms unknown in earlier epochs. Open coiling, planispiral coiling, and umbilici detract from shell sturdiness, and were commoner among Paleozoic and Early Meso- zoic gastropods than among younger forms. Strong external sculpture, narrow elongate aper- tures, and apertural dentition promote resistance to crushing predation and are primarily as- sociated with post-Jurassic mesogastropods, neogastropods, and neritaceans. The ability to remodel the interior of the shell, developed primarily in gastropods with a non-nacreous shell structure, has contributed greatly to the acquisition of these antipredatory features. The substantial increase of snail-shell sturdiness beginning in the Early Cretaceous has accompanied, and was perhaps in response to, the evolution of powerful, relatively small, shell-destroying predators such as teleosts, stomatopods, and decapod crustaceans. A simul- taneous intensification of grazing, also involving skeletal destruction, brought with it other fundamental changes in benthic community structure in the Late Mesozoic, including a trend toward infaunalization and the disappearance or environmental restriction of sessile animals which cannot reattach once they are dislodged. The rise and diversification of angiosperms and the animals dependent on them for food coincides with these and other Mesozoic events in the marine benthos and plankton. The new predators and prey which evolved in conjunction with the Mesozoic reorganiza- tion persisted through episodes of extinction and biological crisis. Possibly, continental breakup and the wide extent of climatic belts during the Late Mesozoic contributed to the conditions favorable to the evolution of skeleton-destroying consumers. This tendency may have been exaggerated by an increase in shelled food supply resulting from the occupation of new adaptive zones by infaunal bivalves and by shell-inhabiting hermit crabs. Marine communities have not remained in equilibrium over their entire geological history. Biotic revolutions made certain modes of life obsolete and resulted in other adaptive zones becoming newly occupied.

An agenda for invasion biology

Here I advocate a comparative and systematic approach in which invasion (the extension of species ranges to areas not previously occupied by that species) is studied from the perspective of individual species as well as of the regions and biotas that export and receive invaders. In order to go beyond the particulars of invasion, it is important to ask: (1) how invaders differ from non-invaders in the arrival, establishment, and integration phases of invasion; (2) how donor regions or communities that have produced many successful invaders differ from those in which few resident species have been able to extend their ranges; (3) how recipient ecosystems with many successfully established invaders differ from those in which few species have taken hold; and (4) how invasion affects evolution not only of the invader itself, but of species in the recipient community with which the invader interacts.

Anatomy of an invasion: the trans-Arctic interchange

When the Bering Strait between Alaska and Siberia opened about 3.5 Ma during the early Pliocene, cool-temperate and polar marine species were able to move between the North Pacific and Arctic-Atlantic basins. In order to investigate the extent, pattern, and dynamics of this trans- Arctic interchange, I reviewed the Recent and fossil distributions of post-Miocene shell-bearing Mollusca in each of five northern regions: (1) the northeastern Atlantic (Lofoten Islands to the eastern entrance of the English Channel and the northern entrance of the Irish Sea), (2) northwestern Atlantic (southern Labrador to Cape Cod), (3) northeastern Pacific (Bering Strait to Puget Sound), (4) northwestern Pacific (Bering Strait to Hokkaido and the northern Sea of Japan), and (5) Arctic (areas north of the Lofoten Islands, southern Labrador, and Bering Strait). I have identified 295 molluscan species that either took part in the interchange or are descended from taxa that did. Of these, 261 are of Pacific origin, whereas only 34 are of Arctic-Atlantic origin. Various analyses of the pattern of invasion confirm earlier work, indicating that there is a strong bias in favor of species with a Pacific origin. A geographical analysis of invaders implies that, although trans-Arctic interchange contributed to a homogenization of the biotas of the northern oceans, significant barriers to dispersal exist and have existed for trans-Arctic invaders within the Arctic-Atlantic basin. Nevertheless, trans-Arctic invaders in the Atlantic have significantly broader geographical ranges than do taxa with a pre- Pliocene history in the Atlantic. Among the possible explanations for the asymmetry of trans-Arctic invasion, two hypotheses were explicitly tested. The null hypothesis of diversity states that the number of invaders from a biota is proportional to the total number of species in that biota. Estimates of Recent molluscan diversity show that the North Pacific is 1.5 to 2.7 times richer than is the Arctic-Atlantic, depending on how faunistic comparisons are made. This difference in diversity is much smaller than is the asymmetry of trans-Arctic invasion in favor of Pacific species. Rough estimates of regional Pliocene diversity suggest that differences in diversity during the Pliocene were smaller than they are in the Recent fauna. The null hypothesis was therefore rejected. The hypothesis of ecological opportunity states that the number of invaders to a region is pro- portional to the number of species that became extinct there. The post-Early Pliocene magnitude of extinction was lowest in the North Pacific, intermediate in the northeastern Atlantic, and probably highest in the northwestern Atlantic. The absolute number and faunistic importance of post-Early Pliocene invaders (including trans-Arctic species, as well as taxa previously confined to warm- temperate waters and western Atlantic species that previously occurred only in the eastern Atlantic) was lowest in the North Pacific, intermediate in the northeastern Atlantic, and highest in the northwestern Atlantic. Further support for the hypothesis of ecological opportunity comes from the finding that hard-bottom communities, especially those in the northwestern Atlantic, show a higher representation of molluscan species of Pacific origin, and are likely to have been more affected by climatic events, than were communities on unconsolidated sandy and muddy bottoms. Support for the hypothesis does not rule out other explanations for the observed asymmetry of trans-Arctic invasion. A preliminary study of species-level evolution within lineages of trans-Arctic invaders indicates that anagenesis and cladogenesis have been more frequent among groups with Pacific origins than among those with Atlantic origins, and that the regions within the Arctic-Atlantic basin with the highest absolute number and faunistic representation of invaders (western Atlantic and Arctic) are the regions in which speciation has been least common among the invaders. The asymmetry of invasion is therefore distinct from the asymmetry of species-level evolution of invaders in the various northern marine regions.

When Biotas Meet: Understanding Biotic Interchange

When the barrier between biotas with long separate histories breaks down, species invade from one biota to the other. Studies of episodes of marine and terrestrial biotic interchange that have occurred during the last 20 million years show that large-scale extinction of species before the onset of interchange renders biotas especially prone to invasion. As environments and species are being exploited and eliminated on an ever increasing scale in the human-dominated biosphere, the geographical expansion of species from biotas in which evolution of high competitive, defensive, and reproductive abilities has proceeded the furthest will become more frequent. Historical events and interactions are essential ingredients for understanding the current and future structure and composition of the worlds biota.

SIZES AND SHAPES OF LIANE LEAVES

We have developed evolutionary models to account for ecological patterns in the size and shape of vine leaves. Leaf size is predicted via an economical model in which photosynthetic gains due to enhanced gas exchange are balanced with the metabolic losses incurred in replacing the concomitant water loss. Mechanical efficiency and appropriate orientation in a light field form the basis of our model for leaf shape. Data from montane rain forest in Venezuela and from varied habitats in Costa Rica illustrate the predicted trends along vertical and horizontal microclimatic gradients. Large, cordate-based leaves with long petioles are favored in sunny situations, while small, narrow-based leaves with short petioles are favored in more shady environments. Compound or deeply lobed leaves of the smallest effective size are expected in the most exposed positions.

Crushing behavior of tropical and temperate crabs

The Guamunian xanthids Carpilius maculatus (L.), C. convexus (Forskal), and Eriphia sebana (Shaw & Nodder), and the parthenopid Daldorfia horrida (L.), possess large master claws with molariform teeth than are used to crush the shells of hermit crabs and snails. These crabs typically sever the spire of their prey, or make a gash in the body whorl. They tend to employ sustained pressure on the prey shell, and, except for Eriphia, rarely attack the outer lip, so that the outer lip of the shell typically remains undamaged, except in shells near the critical size, i.e., the maximum size of vulnerability to predation. Temperate species of Cancer (C. productus Randall and C. oregonensi Rathbun) may also crush shelled prey in the larger of their two claws, but more commonly they use both claws together in breaking open their victims. Sustained pressure is applied for only short periods by these crabs. Gastropod adaptations conferring resistance to crushing by crabs include a thick shell, narrow or otherwise small aperture, thickened outer lip, strong sculpture, and a low spire. Emphasis on these traits lowers the critical size of the prey, i.e., permits escape from cushing at a smaller size. An equatorward increase in the expression of the characteristics of crushing-resistance parallels an increase in crushing power of the crabs.

Economics, volcanoes, and Phanerozoic revolutions

Two intervals of the Phanerozoic stand out as times of biosphere-scale revolution in the sense that biogeochemical cycles came under increased control by organisms. These are the early Paleozoic (extending from just before the Cambrian to the Middle Ordovician, a duration of about 100 m.y.), characterized by the appearance of predators, burrowers, and mineralized skeletons, and by the subsequent diversification of planktonic animals and suspension-feeders; and the later Me- sozoic (latest Triassic to mid-Cretaceous, a duration of somewhat more than 100 m.y.), marked by a great diversification of predators and burrowers and by the rise of mineralized planktonic protists. This paper explores the economic conditions that make such revolutions possible. I argue that opportunities for innovation and diversification are enhanced when raw materials and energy are supplied at increasing rates, or when organisms gain greater access to these com- modities through rising temperatures and higher metabolic rates. Greater per capita availability of resources enables populations to grow; lessens or alters ecological constraints on functional im- provement; makes possible the evolution of high metabolic rates (large incomes), which in turn permit improvement in each of several otherwise incompatible functions; and favors the establish- ment and spread of daughter species arising through founder speciation. Reductions in productivity reinforce adaptational constraints and may bring about extinctions. Massive submarine volcanism, together with its associated phenomena of warming, sea-level rise, and widening of warm-weather zones, is proposed to be the chief extrinsic trigger for the Phan- erozoic revolutions. The later Mesozoic was characterized by continental rifting, which accompanied massive submarine volcanic eruptions that produced large quantities of nutrients and carbon dioxide. This activity began in the Late Triassic and peaked in the mid- to Late Cretaceous. The Early Cambrian was also a time of rifting and may likewise have been marked by large-scale submarine volcanism. Continental and explosive volcanism, weathering, and upwelling are other potential means for increasing evolutionary opportunity, but their effects are either local or linked directly or indirectly with cooling. Intense chemical weathering in the Early Cambrian, however, may have contributed to the early Paleozoic revolution. The extrinsic stimulus was greatly amplified through positive feedback by the evolution of higher metabolic rates and other means for acquiring, trading, retaining, and recycling resources more rapidly and from a wider range of environments. Because these novelties usually require a high and predictable supply of resources, their evolution is more likely when extrinsically controlled supplies increase rather than when per capita availability is low. In the view adopted here, the microevolutionary and microeconomic market forces of competition and natural selection operate against a backdrop of macroeconomic supply and demand. Resources are under both extrinsic and intrinsic control. Positive and negative feedbacks link processes at the micro- and macroeconomic levels. This view complements the genealogical and hierarchical con- ception of evolution by emphasizing that the pattern of descent is influenced by resources and by market forces operating at all scales of space and time.

Intraspecific Shore‐Level Size Gradients in Intertidal Molluscs

A synthesis of new data and literature observations indicates that, when rocky intertidal gastropod species (1) shell size tends to increase in an upshore direction in species characteristic of the littoral fringe and in high intertidal limpets, and (2) shell size often decreases in an upshore direction in species typical of lower intertidal levels. These size gradients are considered to be a response to gradients in the intensity and nature of postlarval prereproductive mortality on the shore. In gastropods whose size gradients are of type 1, mortality generally resulting from physical extremes operates from above and is most effective against small individuals. Among snails with size gradients of type 2, mortality often in the form of predation or other biotic intraction is most intense at low levels. Sedentary species can become graded according to size with shore level only through differential mortality of one size group relative to another over the entire vertical range of the species, while mobile forms may become size segregated by active migration of one size group relative to another.

Formation of the Isthmus of Panama

Independent evidence from rocks, fossils, and genes converge on a cohesive narrative of isthmus formation in the Pliocene. The formation of the Isthmus of Panama stands as one of the greatest natural events of the Cenozoic, driving profound biotic transformations on land and in the oceans. Some recent studies suggest that the Isthmus formed many millions of years earlier than the widely recognized age of approximately 3 million years ago (Ma), a result that if true would revolutionize our understanding of environmental, ecological, and evolutionary change across the Americas. To bring clarity to the question of when the Isthmus of Panama formed, we provide an exhaustive review and reanalysis of geological, paleontological, and molecular records. These independent lines of evidence converge upon a cohesive narrative of gradually emerging land and constricting seaways, with formation of the Isthmus of Panama sensu stricto around 2.8 Ma. The evidence used to support an older isthmus is inconclusive, and we caution against the uncritical acceptance of an isthmus before the Pliocene.