Abstract

The extent to which animal lineages achieve large body size, a trait with broad advantages in competition and defence, varies in space and time according to the supply of (and demand for) resources, as well as the magnitude and effects of extinction. Using the maximum sizes of shallow-water marine shell-bearing molluscs belonging to nineteen guilds (groups of species with similar habits and food sources) in seven temperate regions from the Early Miocene to the Recent, the present study examined the controls on productivity and predation that enable and compel large size to evolve. The North Pacific (especially its eastern sector) has been most favourable to large-bodied species from the Pliocene onward. Large productive kelps (Laminariales) evolved there in conjunction with herbivorous mammals, setting the stage through positive feedbacks between production and consumption for the evolution of large molluscan herbivores and suspension-feeders. The evolution of bottom-feeding predatory mammals together with other large predators created intense selection for large molluscan sizes. Very large molluscs in the Early Miocene were concentrated in the southern hemisphere, especially among metabolically passive species. Extinctions, which preferentially targeted the largest members of guilds in most regions, were more numerous in the southern hemisphere and the North Atlantic than in the North Pacific. Minimal disruption, together with the early evolution of metabolically-active consumers and the positive feedbacks they engendered, accounts for the evolution of molluscan gigantism in the North Pacific.

INTRODUCTION

When humans began to exploit marine shellfish for food at least 164 000 years ago in South Africa (Marean, 2011) and later elsewhere, they encountered many exceptionally large and abundant edible animal species. Had humans instead begun to search for food on temperate seashores during the Oligocene (32 to 23 million years ago), they would have encountered much smaller shellfish. How this potential food source affected (and was affected by) consumers on the demand side and producers on the supply side over geological time is the subject of the present study. The aim is to probe the circumstances that permitted, compelled, and sometimes disallowed large body size to evolve and be maintained in some of the world's most productive and accessible ecosystems. To that end, geographical and historical comparisons are made of shallow-water marine ecosystems from climatically similar times and places aiming to ascertain when, where, in which ecological guilds, and in which clades very large body size evolved and disappeared.

Adult body size evolutionarily integrates predictable aspects of the demand for (and supply of) resources. Demand is created by the costs of doing the work of life (i.e. metabolism) and by natural selection stemming from competition in its broadest sense including predation (Van Valen, 1976) for locally limiting resources. Natural selection results in large size when being larger confers advantages in acquiring and defending sufficient resources to survive and leave offspring. Within a guild (a group of co-occurring species with similar habits, habitats, metabolic rates, and food sources), large-bodied species tend to be competitive dominants that control a disproportionately large fraction of available resources (Brown & Maurer, 1986). In addition, they enjoy a partial refuge in large size from their most potent predators because the costs in time, energy, and risk of injury required for predators to kill and consume victims rise faster than the benefits with increasing prey size (Palmer, 1990). The vulnerable part of the life cycle, when individuals are small and young, is characterized by rapid growth in places that are relatively safe from enemies, as in the pelagic realm, under stones, in a resistant egg capsule or inside the parent's body. In this way, large-bodied species with high metabolic demands reduce the functional trade-offs between traits necessary for survival early in life and the benefits associated with a large body in the reproductive adult stage.

The extent to which selection drives species toward larger body size depends on enabling factors, which control the supply of (and access to) food. The enabling factors that permit large size to evolve in metabolically active species with high demand include: (1) reliably high productivity (the rate at which food is made available); (2) the existence of technology to tap, defend, and capitalize on available resources; (3) high oxygen availability, especially in cold water; and (4) minimal constraints on access to food from either enemies or from excessive heat, cold, turbulence, and toxicity. Maximum adult size in marine animal species is known to increase along geographical gradients of increasing primary productivity in suspension-feeding bivalves, herbivorous gastropods, and many predatory gastropods and crustaceans (Vermeij, 1978, 1980; Bosman, Hockey & Siegfried, 1987; Reaka-Kudla, 2000; Linse, Barnes & Enderlein, 2006; Sejr, Blicher & Rysgaard, 2009). Species with low metabolism and minimal maintenance costs can attain large size under less productive conditions, although they can do so only if mortality during the slow-growing, small-bodied young stages is low. These latter circumstances produce the ‘gentle giant’ syndrome of many soft-bodied Antarctic marine animals (Arnaud, 1974; Rosa & Seibel, 2010) and island tortoises.

The conditions that enable and compel the evolution of large body size in consumers vary in space and time. Suspension-feeders are supported by primary production of phytoplankton, which peaks at mid latitudes, especially in regions where nutrients enter from the land via rivers or are brought up to the sea surface from deep reservoirs by upwelling (Mann, 2000). Herbivores depend on primary production on the seafloor, which, on temperate coasts, is highest where nutrient-rich waters wash over extensive beds of large seaweeds and meadows of seagrass (Mann, 2000). The release of copious dissolved organic matter from living and decaying seaweeds also benefits phytoplankton production (Duggins, Simenstad & Estes, 1989; Mann, 2000). In temperate regions, high primary productivity should therefore allow large-bodied species to evolve among both suspension-feeders and herbivores. On the demand side, basal metabolic rates and the intensity of directional selection for traits that enhance competitive ability and antipredatory defence generally increase with higher temperatures and greater food abundance (Vermeij, 2011a, b). Competition and selection may be intense when food is globally scarce, although the ability of a population to respond to selection is minimal (Vermeij, 2004a). There is mounting evidence that demand, especially predation, stimulates primary production (Vermeij, 2010; Vermeij & Leigh, 2011). Enabling factors, metabolism, and selection are thus connected through strong positive feedbacks between consumers and producers. These feedbacks arise because consumers with large appetites exert strong selection on their victim species in favour of rapid growth and therefore higher biomass turnover and productivity. This selection, in turn, permits consumers to become larger, more abundant, and metabolically more active. These feedbacks may become evolutionarily best developed in regions when production and consumption remain relatively undisturbed for long periods of time.

Large body size becomes disadvantageous when the food supply declines or becomes unstable, or when access to food is restricted by conditions unfavourable to biological activity. These adverse circumstances arise during times of widespread extinction, when primary productivity is reduced and positive feedbacks between producers and consumers are disrupted. Such crises place the largest species in a guild at greatest risk of extinction because it is these species that rely most heavily on a predictably prolific supply of food (Vermeij, 2004b; Vermeij, Dietl & Reid, 2008). Regions in which extinction has been minor should therefore have been most favourable to the evolution of very large size.

In the light of these expected patterns, the present study examined how production and consumption together have affected the evolution of gigantism in bottom-dwelling shallow-water molluscs. As an extension of previous work in the North Atlantic (Vermeij et al., 2008) and the tropics (Vermeij, 2011a), this present study reports and interprets spatial and temporal patterns in maximum body size in molluscan guilds from four northern and three southern temperate regions. No attempt has been made to quantify the roles of supply and demand because doing so implies that these factors act independently, when in fact they are inextricably linked through feedbacks. Instead, the conditions that have influenced production and consumption in each region are analyzed, showing how far selection has driven species in different trophic categories toward gigantism given the enabling factors prevailing on temperate coasts over approximately the last 20 million years.

MATERIAL AND METHODS

The study concentrated on nineteen guilds containing large-bodied species of shallow-water shell-bearing molluscs representing five ecological categories. These are (1) three guilds of grazers (chitons; limpet-like gastropods including haliotids and patellogastropods; and coiled trochoidean and littorinid gastropods); (2) ten guilds of suspension-feeders (byssally attached epifaunal mytilid mussels; oysters and oyster-like cemented bivalves; pectinid scallops; nonsiphonate shallow-burrowing bivalves in Arcoida and Crassatelloidea; siphonate shallow-burrowing veneroidean bivalves; active shallow-burrowing cardiid bivalves; shallow-burrowing active mactrid bivalves; deep-burrowing mactrid and myoidean bivalves; epifaunal calyptraeid slipper limpets; and high-spired epifaunal to shallowly burrowing turritellid gastropods); (3) deposit-feeders (tellinoidean bivalves); (4) chemosymbiotic bivalves (lucinids and thyasirids); and (5) four guilds of predators (drilling soft-bottom naticids; drilling muricids, mainly on hard bottoms; shell-wedging and generalized predatory buccinoidean whelks; and shell-enveloping volutids). These trophic guilds incorporate considerable variation: most large grazers have broad diets that often include sessile animals, as well as primary producers (Otaíza & Santelices, 1985; Briscoe & Sebens, 1988; Camus, Daroch & Opazo, 2008; Sanhueza et al., 2008; Aguilera, 2011); and suspension-feeders take up dissolved organic matter and food particles from the sediment in addition to particulate food suspended in water (Compton et al., 2008).

Although several additional guilds contain notably large species, these are excluded because they have not achieved a cosmopolitan distribution in the temperate zones either in the living biota or in the recent geological past. For example, ranellid gastropods are unknown from the Miocene to the Recent in the north-western Atlantic; byssally attached isognomonid and pinnid bivalves on unconsolidated bottoms have never penetrated the temperate zone in the North Pacific and are absent in the Recent faunas of the north-western Atlantic, South America, and southern Africa. Fast-burrowing razor clams have never lived in New Zealand. Other guilds are analyzed only for certain time intervals because of their restricted distribution at other times. For example, volutid gastropods were temperate-cosmopolitan until the Pliocene but are not represented in the living biotas of the North Atlantic; and shallow-water cardiids are unknown in South America and New Zealand today, even though large-bodied fossil species are prominent in both regions.

Seven temperate regions were considered: four in the northern hemisphere (north-east Atlantic, north-west Atlantic, north-east Pacific, and north-west Pacific) and three in the southern hemisphere (southern Africa, South America, and New Zealand). Most South American data come from the west coast (Peru and Chile) but Argentina, whose biota differs somewhat from that of the Pacific side and where most species do not reach the large sizes of those in western South America, was also considered. The only temperate region not considered is Australia, for which shallow-water faunas comparable to those in other temperate regions are poorly represented in the fossil record. Three time periods were chosen for comparison: the Early to Early Middle Miocene (23 to 16 million years ago), Pliocene (5.3 to 2.5 million years ago), and Recent. A latest Oligocene limpet has been included in the Early Miocene time bin for New Zealand.

Data on the maximum adult shell size (largest linear dimension) of the largest species in each guild, region, and time period were taken from the taxonomic literature, supplemented by specimens in the author's collection and in the following museums: California Academy of Sciences (San Francisco), University of California Museum of Paleontology (Berkeley), Los Angeles County Museum of Natural History, US National Museum of Natural History (Washington), National Museum of Natural History (Leiden), and University Museum of the University of Tokyo. Kazutaka Amano provided some data for Japanese fossil species, and Thomas DeVries and Sven Nielsen supplied additional information about western South American fossils. The largest species of guilds were identified from complete faunal lists and by scanning all available museum collections.

Emphasis on maximum size of the largest species, especially of metabolically active ones, is justified because these species are least constrained (and most benefited) by enabling factors and have been most susceptible to selection by powerful predators (Vermeij et al., 2008; Vermeij, 2011a). The choice was to read the fossil record literally and to ignore potential artefacts and biases associated with preservation and collection effort. Attempts to eliminate or compensate for such sampling problems result in unacceptable loss of data and introduce many new problems.

For each guild and each time interval, temperate regions were assigned a rank according to the maximum size of the largest species, with a rank of 1 representing the largest-bodied species in that guild among the regions considered. Species with 10% of each other's maximum length were assigned the same rank. For example, the largest known living temperate muricids are the north-west Pacific Rapana venosa (Valenciennes, 1846; 190 mm), the north-east Pacific Forreria belcheri (Hinds, 1843; 177 mm), and the western South American Concholepas concholepas (Bruguiére, 1789; 179 mm). All three species were assigned the rank of 2. The next largest species, Dicathais orbita (Gmelin, 1791) from New Zealand, is ranked fourth. For a given time interval, a mean rank was calculated for each region by adding the ranks of each guild and dividing by the number of guilds. All seven temperate regions were considered for the Recent and the Pliocene but, for the Early Miocene, southern Africa was excluded owing to the absence of fossils. To facilitate temporal comparisons, Pliocene rankings of regions were calculated with and without southern Africa.

RESULTS AND DISCUSSION

Maximum size in living faunas

Of the seven living temperate faunas considered, the north-east and north-west Pacific together stand out as housing exceptionally large-bodied species (Tables 1, 2). Guilds whose largest temperate species worldwide occur in the North Pacific (14 of 19, 74%) are found on hard as well as soft bottoms and represent all trophic categories; their number significantly exceeds the 19*(2/7) = 5.4 expected if the largest species were distributed evenly among regions (chi-squared, P < 0.01). At the other end of the spectrum are the two North Atlantic faunas, which lack large coiled herbivorous gastropods, chemosymbiotic bivalves, suspension-feeding turritellids, and predatory muricids. Compared to the north-east Atlantic, the north-west Atlantic supports markedly larger species in eight of 11 guilds on soft bottoms, confirming earlier results (Vermeij et al., 2008). The three southern-hemisphere faunas have mean ranks between those of the two North Pacific and the two North Atlantic faunas (Table 1). Suspension-feeding guilds, however, hold the lowest average rank in western South America, followed closely by southern Africa (Table 1).

Table 1

Mean ranks of temperate regions according to the maximum sizes of the largest species in molluscan guilds

Period and region Mean ranks and number of guilds
 
All guilds Suspension-feeders 
Recent     
North-east Pacific 2.4 16 2.7 
North-west Pacific 2.4 16 2.3 
South America 4.5 16 4.9 
New Zealand 4.5 16 4.6 
Southern Africa 4.3 16 4.8 
North-east Atlantic 5.1 16 4.5 
North-west Atlantic 4.8 16 4.3 
Pliocene with southern Africa     
North-east Pacific 3.2 12 4.1 
North-west Pacific 3.3 12 3.6 
South America 4.3 12 4.5 
New Zealand 3.8 12 3.1 
Southern Africa 4.8 12 5.1 
North-east Atlantic 5.0 12 4.4 
North-west Atlantic 3.5 12 3.1 
Pliocene without southern Africa     
North-east Pacific 2.8 17 3.0 10 
North-west Pacific 3.0 17 3.1 10 
South America 3.9 17 4.2 10 
New Zealand 3.4 17 3.0 10 
North-east Atlantic 4.5 17 4.4 10 
North-west Atlantic 3.4 17 3.6 10 
Early Miocene     
North-east Pacific 3.7 13 4.3 
North-west Pacific 3.3 13 2.9 
South America 2.9 13 2.8 
New Zealand 2.2 13 2.2 
North-east Atlantic 4.0 13 4.7 
North-west Atlantic 3.9 13 3.4 
Period and region Mean ranks and number of guilds
 
All guilds Suspension-feeders 
Recent     
North-east Pacific 2.4 16 2.7 
North-west Pacific 2.4 16 2.3 
South America 4.5 16 4.9 
New Zealand 4.5 16 4.6 
Southern Africa 4.3 16 4.8 
North-east Atlantic 5.1 16 4.5 
North-west Atlantic 4.8 16 4.3 
Pliocene with southern Africa     
North-east Pacific 3.2 12 4.1 
North-west Pacific 3.3 12 3.6 
South America 4.3 12 4.5 
New Zealand 3.8 12 3.1 
Southern Africa 4.8 12 5.1 
North-east Atlantic 5.0 12 4.4 
North-west Atlantic 3.5 12 3.1 
Pliocene without southern Africa     
North-east Pacific 2.8 17 3.0 10 
North-west Pacific 3.0 17 3.1 10 
South America 3.9 17 4.2 10 
New Zealand 3.4 17 3.0 10 
North-east Atlantic 4.5 17 4.4 10 
North-west Atlantic 3.4 17 3.6 10 
Early Miocene     
North-east Pacific 3.7 13 4.3 
North-west Pacific 3.3 13 2.9 
South America 2.9 13 2.8 
New Zealand 2.2 13 2.2 
North-east Atlantic 4.0 13 4.7 
North-west Atlantic 3.9 13 3.4 
Table 2

Maximum sizes in molluscan guilds by period and region

Guild and period Maximum size (mm) by region
 
NEP NWP SAM NZ SAF NEA NWA 
Herbivores        
Chitons        
Recent 350 350 200 87 100 70 50 
Limpets        
Recent 313 210 135 162 190 100 31 
Pliocene 225 200 209 160 148 43 55 
Early Miocene 99 120 50 200 – 29 44 
Coiled gastropods        
Recent 154 130 57 120 132 53 42 
Pliocene 75 85 40 90 70 20 24 
Early Miocene 34 65 – 80 – – 19 
Suspension-feeders        
Turritellids        
Recent 54 80 58 86 106 58 25 
Pliocene 60 110 70 170 47 70 110 
Early Miocene 80 110 110 170 – 35 95 
Slipper limpets        
Recent 57 60 100 62 45 23 59 
Pliocene 108 50 85 76 36 35 65 
Early Miocene 72 75 50 50 – 38 48 
Mussels        
Recent 255 217 208 163 160 220 140 
Pliocene 285 180 100 132 – 150 125 
Early Miocene 135 131 155 182 – – 155 
Nonsiphonate burrowers        
Recent 45 127 40 118 70 70 43 
Pliocene 95 100 47 90 100 90 105 
Early Miocene 44 98 128 153 – 65 81 
Scallops        
Recent 228 200 140 157 106 148 174 
Pliocene 228 220 138 175 – 168 200 
Early Miocene 220 150 200 200 – 75 120 
Veneroids        
Recent 160 127 86 81 88 125 120 
Pliocene 74 95 142 109 97 103 150 
Early Miocene 64 88 98 85 – 74 97 
Matricids        
Recent 155 145 123 111 113 114 175 
Pliocene 85 125 113 84 68 130 130 
Early Miocene 85 101 – – – 10 51 
Deep burrowers        
Recent 280 260 110 121 137 144 183 
Pliocene 200 165 46 160 244 129 135 
Early Miocene 82 111 80 105 – 90 115 
Cardiids        
Recent 140 128 – – – 103 131 
Early Pliocene 105 91 155 155 – 68 68 
Early Miocene 58 102 146 130 – 60 65 
Oysters        
Recent 228 450 50 109 183 180 150 
Pliocene 384 300 217 300 93 100 122 
Early Miocene 113 – 172 136 – 40 184 
Deposit-feeders        
Tellinoids        
Recent 150 135 94 65 85 55 55 
Pliocene 100 126 77 35 72 64 61 
Early Miocene 61 114 54 – – 62 59 
Chemosymbiotic bivalves        
Recent 250 70 – 43 34 40 48 
Pliocene – 76 – 97 – 23 60 
Early Miocene 61 76 78 97 – 31 51 
Predators        
Naticids        
Recent 166 73 85 33 41 38 100 
Pliocene 102 48 44 51 21 50 56 
Early Miocene 59 52 57 70 – 40 48 
Muricids        
Recent 177 190 179 118 83 63 68 
Pliocene 92 50 130 80 110 63 120 
Early Miocene 110 – 45 80 – 93 84 
Volutids        
Recent 125 220 500 205 235 – – 
Pliocene 160 100 200 180 – 200 350 
Early Miocene 170 163 195 135 – 125 73 
Whelks        
Recent 170 210 128 235 237 189 253 
Pliocene 170 169 100 – 101 130 250 
Early Miocene 74 80 110 160 – 99 173 
Guild and period Maximum size (mm) by region
 
NEP NWP SAM NZ SAF NEA NWA 
Herbivores        
Chitons        
Recent 350 350 200 87 100 70 50 
Limpets        
Recent 313 210 135 162 190 100 31 
Pliocene 225 200 209 160 148 43 55 
Early Miocene 99 120 50 200 – 29 44 
Coiled gastropods        
Recent 154 130 57 120 132 53 42 
Pliocene 75 85 40 90 70 20 24 
Early Miocene 34 65 – 80 – – 19 
Suspension-feeders        
Turritellids        
Recent 54 80 58 86 106 58 25 
Pliocene 60 110 70 170 47 70 110 
Early Miocene 80 110 110 170 – 35 95 
Slipper limpets        
Recent 57 60 100 62 45 23 59 
Pliocene 108 50 85 76 36 35 65 
Early Miocene 72 75 50 50 – 38 48 
Mussels        
Recent 255 217 208 163 160 220 140 
Pliocene 285 180 100 132 – 150 125 
Early Miocene 135 131 155 182 – – 155 
Nonsiphonate burrowers        
Recent 45 127 40 118 70 70 43 
Pliocene 95 100 47 90 100 90 105 
Early Miocene 44 98 128 153 – 65 81 
Scallops        
Recent 228 200 140 157 106 148 174 
Pliocene 228 220 138 175 – 168 200 
Early Miocene 220 150 200 200 – 75 120 
Veneroids        
Recent 160 127 86 81 88 125 120 
Pliocene 74 95 142 109 97 103 150 
Early Miocene 64 88 98 85 – 74 97 
Matricids        
Recent 155 145 123 111 113 114 175 
Pliocene 85 125 113 84 68 130 130 
Early Miocene 85 101 – – – 10 51 
Deep burrowers        
Recent 280 260 110 121 137 144 183 
Pliocene 200 165 46 160 244 129 135 
Early Miocene 82 111 80 105 – 90 115 
Cardiids        
Recent 140 128 – – – 103 131 
Early Pliocene 105 91 155 155 – 68 68 
Early Miocene 58 102 146 130 – 60 65 
Oysters        
Recent 228 450 50 109 183 180 150 
Pliocene 384 300 217 300 93 100 122 
Early Miocene 113 – 172 136 – 40 184 
Deposit-feeders        
Tellinoids        
Recent 150 135 94 65 85 55 55 
Pliocene 100 126 77 35 72 64 61 
Early Miocene 61 114 54 – – 62 59 
Chemosymbiotic bivalves        
Recent 250 70 – 43 34 40 48 
Pliocene – 76 – 97 – 23 60 
Early Miocene 61 76 78 97 – 31 51 
Predators        
Naticids        
Recent 166 73 85 33 41 38 100 
Pliocene 102 48 44 51 21 50 56 
Early Miocene 59 52 57 70 – 40 48 
Muricids        
Recent 177 190 179 118 83 63 68 
Pliocene 92 50 130 80 110 63 120 
Early Miocene 110 – 45 80 – 93 84 
Volutids        
Recent 125 220 500 205 235 – – 
Pliocene 160 100 200 180 – 200 350 
Early Miocene 170 163 195 135 – 125 73 
Whelks        
Recent 170 210 128 235 237 189 253 
Pliocene 170 169 100 – 101 130 250 
Early Miocene 74 80 110 160 – 99 173 

NEA, north-east Atlantic; NEP, north-east Pacific; NWA, north-west Atlantic; NWP, north-west Pacific; NZ, New Zealand; SAF, southern Africa; SAM, South America.

Maximum size is greater in at least one tropical region, which is usually the Indo-West Pacific or eastern Pacific (Vermeij, 2011a), than in any temperate area in eight guilds (low-coiled hard-bottom grazing gastropods, chemosymbiotic lucinids, inactive turritellid and nonsiphonate burrowing bivalves, cockles, and predatory muricids, whelks, and volutids). Guilds with very large-bodied species in the tropics that are only sporadically represented or entirely absent from temperate regions include high-spired and stromboidean herbivores, cowrie-like gastropods, worm-eating gastropods, and echinoderm-feeders. Guilds that reach larger sizes in one or more temperate regions include chitons, limpets feeding on fleshy seaweeds, suspension-feeders in seven guilds (mussels, scallops, oysters, mactrids, veneroids, deep-burrowing bivalves, and slipper limpets), deposit-feeding tellinoideans, and predatory naticids. These geographical patterns reflect the greater abundance and productivity of phytoplankton and the larger size of fleshy seaweeds in the temperate zones.

Size patterns in the past

The distribution of maximum size among temperate regions has changed substantially over the course of the last twenty million years. During the Early Miocene, the largest temperate species in most (13 of 18) guilds lived in the southern hemisphere (New Zealand and South America), representing more than twice the number that would be expected from a random distribution of maximum sizes across regions (chi-squared, P < 0.01). The two North Atlantic regions occupy the lowest rank: the number of guilds with the smallest maximum size in either the north-east or north-west Atlantic (ten of 18) is significantly higher than the six expected (chi-squared, P < 0.05). In the Early Pliocene, the two North Pacific regions hold the top ranks of all guilds taken together but, with predatory guilds treated separately, the north-west Atlantic ranks highest (Table 1). Overall, the largest temperate Pliocene species are distributed evenly across regions. From the Early Miocene to the Recent, there is a general northward shift in gigantism from the southern hemisphere to the North Pacific.

Temporal trends in maximum body size within guilds can be characterized either as increases (including cases of no significant change) or decreases. From the Early Miocene to the Pliocene, maximum size increased in a majority of guilds in all regions (Table 3). The number of increases significantly exceeds the number of decreases in the four northern regions (chi-squared, P < 0.01) but not in the two southern ones. From the Pliocene to the Recent, increases outnumbered decreases in most regions but significantly so only in the north-west Pacific (Table 3). The north-west Atlantic is the only region where maximum size decreased in a majority of guilds (nine versus eight). From the Early Miocene to the Recent, increases in maximum size exceeded decreases significantly (chi-squared, P < 0.05) in the north-east and north-west Pacific and in the north-east Atlantic but did not do so in South America or the north-west Atlantic; in New Zealand, decreases slightly outnumbered increases (Table 3).

Table 3

Proportion of decreases in maximum body size in guilds

Interval and region Number of decreases/total number of guilds 
Pliocene to Recent  
North-east Pacific 6/17 = 0.35 
North-west Pacific 1/17 = 0.059 
South America 5/16 = 0.31 
New Zealand 8/17 = 0.47 
Southern Africa 4/13 = 0.31 
North-east Atlantic 7/16 = 0.44 
North-west Atlantic 9/16 = 0.56 
Early Miocene to Pliocene  
North-east Pacific 2/17 = 0.12 
North-west Pacific 4/16 = 0.25 
South America 7/15 = 0.47 
New Zealand 6/16 = 0.37 
North-east Atlantic 3/16 = 0.19 
North-west Atlantic 2/18 = 0.11 
Early Miocene to Recent  
North-east Pacific 3/18 = 0.17 
North-west Pacific 1/16 = 0.06 
South America 5/14 = 0.36 
New Zealand 9/15 = 0.60 
North-east Atlantic 4/15 = 0.27 
North-west Atlantic 8/18 = 0.44 
Interval and region Number of decreases/total number of guilds 
Pliocene to Recent  
North-east Pacific 6/17 = 0.35 
North-west Pacific 1/17 = 0.059 
South America 5/16 = 0.31 
New Zealand 8/17 = 0.47 
Southern Africa 4/13 = 0.31 
North-east Atlantic 7/16 = 0.44 
North-west Atlantic 9/16 = 0.56 
Early Miocene to Pliocene  
North-east Pacific 2/17 = 0.12 
North-west Pacific 4/16 = 0.25 
South America 7/15 = 0.47 
New Zealand 6/16 = 0.37 
North-east Atlantic 3/16 = 0.19 
North-west Atlantic 2/18 = 0.11 
Early Miocene to Recent  
North-east Pacific 3/18 = 0.17 
North-west Pacific 1/16 = 0.06 
South America 5/14 = 0.36 
New Zealand 9/15 = 0.60 
North-east Atlantic 4/15 = 0.27 
North-west Atlantic 8/18 = 0.44 

The six guilds of sedentary suspension-feeders as adults (turritellids, slipper limpets, mussels, scallops, oysters, and nonsiphonate burrowers) show a larger number of decreases in maximum size than the four guilds of suspension-feeders in which individuals are either mobile or produce powerful feeding currents (veneroids, mactrids, cockles, and deep burrowers). From the Pliocene to the Recent, decreases account for 24 of 41 cases (59%) in the sedentary group and only five of 25 cases (20%) in the active group (chi-squared, P < 0.01). From the Early Miocene to the Pliocene, the trend is the same but is not quite statistically significant at the 0.05 level: sedentary guilds witnessed decreases in maximum size in 13 of 35 cases (37%), whereas active guilds saw decreases in only two of 22 cases (9.1%). A similar difference between passive and active suspension-feeding guilds was noted for size patterns in the Late Neogene tropics (Vermeij, 2011a).

Overall, these data indicate that maximum size increased most consistently and to the greatest extent in the North Pacific. They therefore suggest that conditions in the North Pacific (i.e. high productivity, intense selection by enemies, and minimal disruption) were particularly favourable for the evolution and maintenance of very large size in shallow-water molluscs.

The role of productivity

Planktonic production and suspension-feeding

The temperate regions with the highest estimated planktonic primary productivity (up to 800 g C m–2 year–1) are the upwelling zones in the Benguela Current system off southwestern Africa and the Humboldt Current system off Peru and northern Chile (Walsh, 1988; Mann, 2000). These are not, however, the regions with the largest suspension-feeding molluscs. In fact, the mean rank of nine suspension-feeding guilds in southern Africa (4.7) and western South America (5.1) are the lowest among the seven regions considered (Table 1). These same regions rank lowest among suspension-feeders in the Early Pliocene as well, when intense upwelling was already a prominent feature of ocean conditions there (Dunbar, Marty & Baker, 1990; Diesterh-Haass, Meyers & Vidal, 2002; Heinrich et al., 2011; Rommerskirchen et al., 2011). The upwelling systems of the California Current in the north-east Pacific are less productive (150 g C m–2 year–1) but support the next-to-largest suspension-feeders (mean rank 2.7). The upwelling regime in California has existed with varying intensities since Late Miocene times (Barron, 1998; Jacobs, Haney & Louie, 2004) but upwelling may have been reduced (or been less effective at bringing up nutrients from deep water) during the Early Pliocene; yet the mean rank of suspension-feeding guilds in the Early Pliocene north-east Pacific is tied for highest place when South African data are excluded (Table 1).

A possible explanation for the lack of correspondence between maximum size of suspension-feeders and estimated planktonic productivity is that peak production and nutrient concentrations in upwelling regions occur well offshore (Barber, 1988; Walsh, 1988; Mann, 2000), whereas the suspension-feeders are found nearshore in shallow subtidal and lowest intertidal habitats. Unpredictability in the intensity of upwelling, nutrient levels, and planktonic productivity from year to year may be another contributing factor, especially on the west coast of South America, where normally high rates of production plummet during EI Niño-Southern Oscillation events (Barber, 1988). The largest suspension-feeding mussels, barnacles, and burrowing bivalves in western South America are found not in the zone of upwelling but in the quiet waters of southern Chile, where strong tidal currents sweep nutrients over the bottom but upwelling does not occur. In the Late Miocene and Early Pliocene of California, exceptionally large mussels, scallops, oysters, and slipper limpets are found in embayments and in the inland sea of the San Joaquin Basin, where nutrient enrichment occurs by the incursion of waters from the adjacent open Pacific Ocean (Kirby, 2001; Bowersox, 2005). Embayments and lagoons were also much more extensive on the western coast of South America during the Early Pliocene, when sea levels were higher and uplift of the coast had not proceeded as far (Dunbar et al., 1990).

Benthic productivity and herbivory

Benthic primary productivity in the temperate zones is 1.5 to 10 times higher than planktonic productivity (Smith, 1981; Mann, 2000; Worm, 2000) and is concentrated nearshore. By releasing large quantities of dissolved organic matter, which is subsequently absorbed by bacteria or coagulated into particles and therefore accessible to suspension-feeders (Duggins et al., 1989; Mann, 2000), algal primary producers on the seafloor contribute to the food supply of all shallow-water consumers. On temperate coasts, therefore, benthic producers should have a greater overall influence on primary consumers (suspension-feeders as well as herbivores) than pelagic producers.

The highest estimated rates of benthic production are for kelps of the genus Postelsia in Washington State in the north-east Pacific (Leigh et al., 1987; 8.6 kg C m–2 year–1), although even higher rates are likely in the absence of herbivores (Paine, 2002). Typical rates of primary production by large seaweeds along temperate coasts range from 1.0 to almost 1.8 kg C m–2 year–1 (Mann, 2000), with north-east Atlantic maxima being somewhat lower than those in the north-west Atlantic, north-east Pacific, southern Africa, and temperate Australia. Productivity of temperate seagrass beds is less well known, although the highest estimates are 0.8 kg C m–2 year–1 for Zostera meadows in Denmark (Mann, 2000). From these estimates, the north-east Pacific might be expected to support the largest herbivores and suspension-feeders, as is indeed the case (Tables 1, 2). Questions remain, however, about how regional differences in productivity and herbivory have arisen.

Very large brown seaweeds, which account for the highest rates of primary production on temperate coasts, arose in only two regions. Kelps (order Laminariales) originated in the North Pacific, with the largest species evolving on its eastern side. By the Early Pliocene at the latest, kelps had spread to the North Atlantic, southern Africa, South America, and temperate Australasia (Estes & Steinberg, 1988; Coyer, Smith & Andersen, 2001; Lane et al., 2006). The fucoid Durvillaea likely arose in the southwestern Pacific and has subsequently spread to western South America (Fraser et al., 2010).

The North Pacific is also the only region where seaweed-eating marine mammals evolved. Land-derived desmostylians, which lived on North Pacific shores from the Early Oligocene to the Late Miocene (Domning, Ray & McKenna, 1986; Ray, Domning & McKenna, 1994; Beatty, 2009), are inferred to have fed on seagrasses, although some species may also have included algae in their diet (Domning, 1989; Clementz, Hoppe & Koch, 2003). Seagrass feeding sirenians of the genus Dusisiren extended to the north-east Pacific from warmer American waters during the Early Middle Miocene and had spread to Japan by the Late Miocene. By the Early Pliocene, one lineage of Dusisiren had given rise to the much larger Hydrodamalis, represented in the Recent fauna by Hydrodamalis gigas, a species hunted to extinction by humans (Domning, 1976, 1978; Takahashi, Domning & Saito, 1986).

Kelps differ from other seaweeds by their rapid growth, high productivity, large standing crop, nutrient storage, and vascular system (Mann, 1973; Mann, Chapman & Gagné, 1980). These traits may have evolved in response to natural selection by endothermic herbivores with large appetites (Vermeij, 2004a, 2010). Seaweed-eating marine mammals are unknown outside the North Pacific. Many anseriform birds (geese, swans, and ducks) feed on seagrasses, and some gulls (Larus) and geese (Branta in the northern hemisphere, Chloephaga in southern South America) occasionally consume ephemeral algae (Summers & Grieve, 1982; Hori, Noda & Nakao, 2006), although specialized kelp-eating birds have not evolved. Mammals therefore appear to be largely responsible for the evolution of highly productive seaweeds in the North Pacific.

In southern New Zealand, Durvillaea is consumed by the large (45 cm) wrasse Odax (Taylor & Schiel, 2010), which belongs to a lineage originating approximately 38 Mya during the Late Eocene (Clements et al., 2004). Species of the southern-hemisphere lobster genus Jasus consume large brown seaweeds on islands in the southern Indian and Atlantic Oceans (Beurois, 1975) and may well do so in southern Africa, South America, and New Zealand as well. One or more of these large ectothermic herbivores may thus have influenced the evolution and adaptive characteristics of Durvillaea.

The ability of some abalones (Haliotis spp.), South African limpets (Cymbula spp.), and sea urchins to capture and consume large drifting seaweeds not only increased the effective productivity and stock of algal foods (Bustamante, Branch & Eekhout, 1995), but also could have contributed to the evolution of large size in these herbivores, as suggested for kelp-eating abalone by Estes, Lindberg & Wray (2005). Consumption of large drifting seaweeds is known in the North Pacific, South Africa, South America, and New Zealand (Branch, 1971; Tegner, 1980; Duggins, 1981; Moreno & Sutherland, 1982; Dayton, 1985; Vásquez & Buschmann, 1997).

It is noteworthy and puzzling that the presence of productive kelps and high-shore fucoids elicited feeding specialization by small littorinid and patellid gastropods in the north-eastern Atlantic (Vermeij, 1992) but did not lead to the evolution of large herbivores anywhere in the North Atlantic. Although the north-eastern Atlantic limpet Patella vulgata Linnaeus, 1758, can trap and feed on drifting upper-shore fucoids (Lorenzen, 2007), no North Atlantic herbivorous mollusc is sufficiently large to catch and eat drifting kelp.

In short, very large herbivorous molluscs arose in regions where other high-energy herbivores (mammals in the North Pacific, fish in the southwestern Pacific) selected for fast-growing, large seaweeds, and where the ability to capture drifting kelps evolved. The region with the largest seaweeds, highest-energy herbivores, and most diverse herbivores capable of trapping drifting kelps is the North Pacific.

Despite their high productivity and the presence of endothermic herbivorous mammals and birds since the Early Oligocene in the North Pacific and the Miocene in the North Atlantic and South America, temperate seagrass meadows lack herbivorous molluscs greater than 15 mm in length. This situation contrasts markedly with tropical seagrass communities, which have supported herbivorous gastropods of 100 mm length or more from the Early Eocene onward (Vermeij, 2011a). The reasons for this contrast remain unclear.

Predation

If competition among, and selection by, predators is a primary agency in the evolution of large body size in prey species, the spatial and temporal patterns in maximum body size described in the present study would imply that: (1) predation is most intense, or has been least constrained, in the north-east Pacific and most encumbered in the North Atlantic and (2) predators have become increasingly powerful agents of selection on many temperate shores since Early Miocene times, especially in the North Pacific. As shown below, there is substantial but not complete support for these predictions.

The north-east Pacific stands out as a region with exceptionally large and diverse predators of shell-bearing molluscs. The largest species worldwide in four guilds of ectothermic predators in addition to drilling naticid gastropods are found in the north-east Pacific: octopods (Enteroctopus dofleini, with a lateral spread of 9.6 m and weighing up to 330 kg; Newman, 1994); sea stars ingesting whole prey (Pycnopodia helianthoides, subtidal individuals up to 1.5 m in diameter; Mauzey, Birkeland & Dayton, 1968); sea stars using force to open bivalves (Pisaster ochraceus, subtidal individuals at least 45 cm in diameter and weighing more than 3 kg; Paine, 1976); and cancrid crabs (Cancer productus, up to 267 mm wide; Harrison & Crespi, 1999).

Endothermic predators capable of eating large molluscan prey have evolved only in the North Pacific, the western coast of South America, and as minor players in the north-west Atlantic. The earliest to do so were Early Miocene amphicynodontid bear-like carnivores of the genus Kolponomos in the north-east Pacific. According to Tedford, Barnes & Ray (1994), they had shell-crushing dentition and strong neck musculature consistent with a diet of large intertidal molluscs. The otariid seal Gomphotaria from the Late Miocene of southern California was likely also a shellcrusher (Barnes & Raschke, 1991). Walruses (Odobenidae), which feed on burrowing bivalves by using suction to remove the soft parts from the shell (Lowry, Frost & Burns, 1980; Oliver et al., 1983; Fukuyama & Oliver, 1985), have Early Middle Miocene origins in the North Pacific (Deméré & Berta, 2001; Kohno, 2006), although when fish-eating was replaced by benthic predation on molluscs in this group remains unknown. The sea-otter genus Enhydra in the Mustelidae is a member of an Old World clade of otters that likely became marine in the north-west Pacific (Koepfli et al., 2008). It preys on sea urchins, large rocky-shore and soft-bottom molluscs, and many other animals (Calkins, 1978; VanBlaricom, 1988; Kvitek et al., 1992) on both sides of the North Pacific. The fossil record of Enhydra (Willemsen, 1992) begins in the earliest Pleistocene.

On the western temperate coast of South America, the sea otter Lontra felina (Molina, 1782) is an important shell-crushing predator of large molluscs on exposed rocky shores (Castilla & Bahamondes, 1979). Phylogenetic analyses show this species is derived from a Patagonian lineage of otters that became marine in the Late Pleistocene (Koepfli et al., 2008; Vianna et al., 2010, 2011).

Three lineages of benthically feeding marine mammals are known from the North Atlantic, although only one originated there and none survives on temperate Atlantic shores. The walrus lineage (Odobenus) entered the Atlantic during the Early Pliocene and persists in the Arctic sector (Repenning, 1976). Enhydra was present in the Pleistocene of the North Sea Basin (Willemsen, 1992). An Early Pleistocene occurrence of Enhydra in Arctic Alaska (Hopkins & Marincovich, 1984; Carter et al., 1986) supports the hypothesis that Enhydra entered the temperate Atlantic by way of the Arctic from the North Pacific. Finally, the eastern North American sea mink (Mustela macrodon) became an intertidal shell-crusher during the latest Pleistocene or Holocene and has become extinct in historic time (Waters & Ray, 1961; Sealfon, 2007). The bearded seal (Erignathus barbatus) has a broad diet including small molluscs (Lowry et al., 1980; Marshall, Kovacs & Lydersen, 2008). This mainly Arctic species, which extends into the northern Bering Sea as well, has not invaded the temperate waters of the Atlantic and is not considered further here.

Although birds are important endothermic predators of molluscs and other shore animals in all temperate and polar regions, their small size and limited capacity to handle large prey make birds poor candidates as major agents of selection favouring large size in molluscs. The birds capable of taking the largest prey (i.e. gulls, oystercatchers, crows, and eider ducks of the genus Somateria) are limited to prey smaller than 55 to 73 mm in maximum dimension (Webster, 1941; Harris, 1965; Norton-Griffiths, 1967; Brun, 1971; Dunthorn, 1971; Baker, 1974; Hartwick, 1976; Zach, 1978; Hockey & Branch, 1984; Lindberg, Warheit & Estes, 1987; Cadée, 2008a, b). This upper size limit is smaller than that of co-occurring predators such as sea otters, muricids, anticids, large whelks, octopods, lobsters, crabs, and sea stars that use force to open bivalves. Other molluscivorous birds are restricted to much smaller prey (Navarro, Velasquez & Schlatter, 1989; González, Piersma & Verkuil, 1996; Piersma et al., 2003; Cadée, 2011).

Ectotherms, especially sea stars and crustaceans, are likely to be important agents of selection for large size in molluscan prey in all temperate regions. In South America, they include species of the crab genus Cancer, the octopod Enteroctopus, and sea stars of the genera Heliaster and Meyenaster, as well as muricid gastropods and, on the Patagonian coast, large volutids (Dayton et al., 1977; Ortiz et al., 2003; Escobar & Navarrete, 2011). In New Zealand, where no molluscivorous marine mammals occur, the top predators of molluscs are clawless palinurid lobsters of the genus Jasus and the sea star Stichaster. Southern Africa also lacks marine mammals; top predators there include Jasus and the sea star Marthasterias (Griffiths & Seiderer, 1980; Butler, Steneck & Herrnkind, 2006). Finally, in the North Atlantic, the largest living molluscivores are cod and clawed nephropid lobsters of the genus Homarus (Butler et al., 2006).

In summary, the available evidence indicates that large endothermic predators capable of eating large molluscs appeared early in the North Pacific, and much later if at all in other temperate regions. These predators may account for the very large size of species in many molluscan and non-molluscan guilds in the North Pacific. It remains a mystery, however, which selective agents were responsible for the large size of many Miocene species in the southern hemisphere.

Extinction and size

The magnitude of species-level extinction among molluscs since the Early Pleistocene in the temperate marine realm varies from a low of 30% to 39% in the north-east and north-west Pacific (Stanley, 1986b; Bowersox, 2005), to highs of 79% in the north-west Atlantic (Vermeij et al., 2008) and 83% to 88% in South America (Guzmán et al., 2000; Rivadeneira & Marquet, 2007). The Spearman rank correlation between the post-Pliocene magnitude of extinction and the mean rank of the largest species in Recent guilds in the seven regions is −0.72, indicating that extinction interferes with the evolution of large body size. Indeed, extinction was more severe among the largest members of guilds than among molluscs as a whole in all temperate regions except South America, confirming previous work in the North Atlantic (Vermeij et al., 2008). Pliocene to Early Pleistocene giants had magnitudes of extinction varying from 56% in the north-west Pacific and 76% in the north-east Atlantic to 88% in the north-west Atlantic and 94% in New Zealand. Stanley (1986a) previously suggested that Pliocene extinctions in the warm-temperate western Atlantic were not size-biased; and Smith & Roy (2006) showed that large north-east Pacific scallops had, on average, a lower magnitude of extinction than smaller species. The latter study, however, included several species in their largest size class. Reexamination of their data shows that the single largest species in each Pliocene guild was more prone to extinction than other large species, consistent with the present findings.

Several large-shelled taxa became extinct during or after the Pliocene without being replaced by modern equivalents. They include the pteriodean bivalves Hippochaeta in the north-west Atlantic, Neopanis in New Zealand, and ‘Isognomon’ in Chile and South Africa; the large New Zealand cardiid Maoricardium; and the volutids Volutifusus in the north-west Atlantic and ‘Scaphella’ in the north-east Atlantic. The inclusion of these taxa would have made the difference between the magnitude of extinction of the largest members of guilds and that of molluscs as a whole even more stark. It is noteworthy that all these unreplaced taxa, as well as other large-bodied species that became extinct and were ecologically replaced by large species in different clades, lived in nutrient-rich lagoons and bays, environments that were largely obliterated in the north-east Pacific and in western South America (Jacobs et al., 2004; Bowersox, 2005; Kiel & Nielsen, 2010).

Clade identity and contingency

The identity of clades to which the largest members of a guild belong varies both in space and over time. In the guild of living limpet-like herbivores, for example, the largest species belong to Fissurellidae in South America, to a clade within Haliotidae in the North Pacific, and to a separate haliotid clade in New Zealand and southern Africa (Estes et al., 2005). Among scallops, comprising the single clade Pectinidae, the largest living species belong to the clades Pectinini (Pecten in New Zealand, South Africa, and the north-east Atlantic), Palliolini (Placopecten in the north-west Atlantic), Aequipectinini (Argopecten in western South America), and Chlamydini (Mizuhopecten in the north-west Pacific, Patinopecten in the north-east Pacific). In the Pliocene, still other pectinid subclades contained the largest species: Mesopeplini (Phialopecten in New Zealand), Decatopectinini (Lyropecten in the north-east Pacific), and a separate clade within Palliolini (Pseudamussium in the north-east Atlantic; for phylogeny, see Waller, 2006).

Of the 19 guilds examined in the present study, eight comprise large-bodied species for which a robust phylogenetic hypothesis has been proposed. Of the 144 species in these eight guilds (42% of the 347 largest-bodied species considered in the present study), 84 (58%) represent distinct clades, in which large size evolved independently. The present study identified 85 cases of temporal succession of phylogenetically well characterized species within guilds. Of this number, 51 (60%) represent clear instances of temporal clade substitution among largest-bodied species within a guild. These data strongly indicate that lineages hold the status of largest-bodied member of a guild within a region only briefly, and that phylogenetic usurpation of this top status is the rule.

The largest Pliocene and Recent members of guilds in a region usually belong to clades with a long history in that region. Of 125 Recent species, only ten (8.0%) are immigrants from elsewhere, nine from the North Pacific to the North Atlantic, and one (Pecten) from South Africa to New Zealand via Australia (Vermeij, 1991; Beu, 2004). Without the North Pacific immigrants, decreases in maximum size from the Pliocene to the Recent would have outnumbered increases by 12 : 5 instead of 9 : 8 in the north-west Atlantic and by 11 : 5 instead of 7 : 9 in the north-east Atlantic. Clades of large-bodied non-molluscan predators and herbivores show the same pattern of long history in most regions and recent immigration to the North Atlantic. Fossil and phylogenetic evidence indicates that large North Pacific and southern-hemisphere forcipulate sea stars, North Atlantic gadid fishes including cod, North Atlantic and southern-hemisphere lobsters, north-east Pacific cancrid crabs, and the herbivorous mammals and wrasses discussed earlier all belong to clades with long pre-Pliocene histories in their respective regions (Harrison & Crespi, 1999; Patek et al., 2006; Teletchea, Laudet & Hanni, 2006; Mah & Foltz, 2011). Newcomers include sea otters (see above) and North Atlantic forcipulate sea stars (Mah & Foltz, 2011), large cancrid crabs (Harrison & Crespi, 1999), sea mink, and walrus (see above). The cod Gadus morhua, although it belongs to the clade Gadinae with a long Atlantic history, may represent a re-invasion to the North Atlantic by a lineage that had previously entered the North Pacific via the Arctic Ocean (Coulson et al., 2006). Geologically recent immigration from the North Pacific by large-bodied molluscs and many of their enemies thus partially reversed the effects of widespread Pliocene and Early Pleistocene extinctions in the North Atlantic.

These data support the general conclusion that a given trait with a large, broadly adaptive advantage (i.e. large size in the present case) is very much less contingent on the unique events and circumstances of history than are the identities of the clades with that trait or the sources of selection favouring the trait. Of the many clades in which the potential for evolving large body size exists, only a few achieve the highest size rank in their respective guilds. Which clades are involved and which are responsible for pushing them there depends on quirks of geography and on the fates of potential competitors. In short, the outcomes and directions of evolution are more predictable than the players in the evolutionary drama (Vermeij, 2006, 2010, 2011c).

Conclusions

Even under climatically similar circumstances, biotas in different parts of the world have separate histories and often diverge from one another in the prevailing biological conditions that the resident species respond to and create. Comparative studies of the kind undertaken in the present study not only help to identify similarities and contrasts between biotas that have developed independently, but also expose long-term evolutionary agencies (i.e. ecological feedbacks, natural selection and its consequences, and extinction) that shape the composition of, and relationships in, those biotas. They show that current conditions are insufficient to explain the heterogeneity we observe on biogeographical scales.

Many questions remain. Why did metabolically active herbivorous and predatory marine mammals that feed on bottom-dwelling organisms emerge so early in the north Pacific and so late or not at all elsewhere? What accounts for the large differences among regions in the magnitude of extinction during the Pliocene? Why are there gigantic worm-eating, echinoderm-feeding, and soft-bottom herbivorous gastropods in the tropics and not in the temperate zones? Given the widely held view that dispersibility in the sea is high, why have so few competitively dominant species and the larger clades to which they belong so often remained in one or two regions without spreading more widely as successful invaders?

These and other biogeographical and evolutionary questions require more insights into the biology of individual species and communities. Satisfactory answers will also require a better understanding and measurement of productivity. Finally, it is essential to recognize that a given regime of production or selection does not affect all species in the same way. Some species will have the technology to harvest resources even when other species do not; and prior adaptation greatly affects how a given species responds evolutionarily to a predator. In simplified theoretical models, such heterogeneity is often ignored or relegated as noise. In the real world of economic relationships among organisms, heterogeneity is a key property that must be analyzed and celebrated if we are to understand the processes of history.

ACKNOWLEDGEMENTS

I thank Tova Michlin and my wife Edith for technical assistance; as well as Patricio Camus, Thomas DeVries, David Lindberg, Sven Nielsen, Ricardo Otaiza, Theunis Piersma, and Peter Wainwright for helpful discussions.

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