Shifting sources of productivity in the coastal marine tropics during the Cenozoic era

Abstract

Changes in the rates and sources of marine primary production over time are difficult to document owing to the absence of direct estimates of past productivity. Here, I use the maximum body sizes of the largest species in each of 23 tropical shallow-water marine molluscan guilds (groups of species with similar habits and trophic roles) to trace the relative importance of planktonic and benthic primary productivity from the Eocene (55 Ma) onwards. The largest members of guilds are least constrained in exploiting resources and therefore reflect the availability and accessibility of those resources most accurately. Maximum sizes of suspension-feeders and predators increased by a factor of 2.3 and 4.0, respectively, whereas those in four out of five herbivorous guilds declined. I interpret these patterns, which are discernible throughout the coastal tropics, to mean that primary production in the Eocene marine tropics was concentrated on the seafloor, as is the case today on offshore reefs and islands, and that the Miocene to the recent interval witnessed a dramatic increase in planktonic productivity along continental margins. The rise in planktonic fertility is best explained by an increase in nutrient supply from the land associated with intense global tectonic activity and more vigorous ocean mixing owing to cooling.

1. Introduction

Organisms in nature face a constellation of conditions that are broadly divisible into enabling factors—resources and the circumstances that make them available and accessible—and agencies that threaten survival and propagation. Adaptations reflect predictable aspects of these enabling factors and selective agencies, and evolutionary trends chronicle changes in both. In evolutionary studies of ancient species, the contribution of enabling factors has received little attention, because direct estimates of rates of primary production, on which all members of ecosystems depend, have proven difficult to obtain. Recent work on leaf venation in land plants [1,2] has for the first time made estimates of past photosynthetic capacity in land plants possible, but inferences about marine productivity based on carbon-isotopic ratios [3] are afflicted by many artefacts and difficulties of interpretation and are less compelling.

A novel way of assessing the availability and accessibility of resources is to interrogate those consumers that, by virtue of their competitive superiority, are least constrained in exploiting those resources. Threats from competitors, predators and the weather limit access to resources, but these threats are reduced for competitively dominant species. Because large adult size typically confers competitive superiority and high demand for resources within a guild of species with similar habits and trophic roles, maximum body size of the largest species in a guild is a good indicator of resource supply as perceived by the organism itself given the individual's mobility, metabolic demand and feeding-related machinery [4]. Comparisons of maximum body sizes among co-occurring guilds can thus reveal the relative contributions of the various sources of production (such as phytoplankton and benthic plant-like organisms), whereas comparisons of maximum sizes within a guild over time track changes in the productivity of a given class of resources. Such comparisons apply only to permanent communities of species whose individuals have long life spans; they are invalid for ephemeral, highly disturbed systems, such as those prevailing after mass extinctions, in which most individuals are small, fast-growing, short-lived opportunists.

By emphasizing maximum body size within guilds, I avoid the ecological heterogeneity and sampling problems that are inherent in comparisons involving the size distributions of whole faunas. For most species, interference competition from large-bodied species limits resource acquisition and may select against large size. These species, which comprise the vast majority in a community, are thus not ecologically equivalent to top competitors. From the perspective of sampling, large-bodied species are more easily collected and better known than their smaller counterparts. Moreover, previous work [4] indicates that maximum size is not correlated with overall diversity, a finding also supported in the present study.

Primary consumers in shallow-water marine ecosystems are broadly classifiable as planktivores, which feed on organisms suspended in water, and herbivores, which consume bottom-dwelling (benthic) photosynthesizing organisms. Most primary production in clear, plankton-poor (oligotrophic) waters occurs in the benthos, where the principal contributors in the tropics are low-growing algae, photosymbiotic animals, and seagrasses, depending on the consistency of the bottom [5–7]. The largest and most abundant primary consumers in benthic oligotrophic environments are herbivores and, where plant-derived nutrients accumulate in sediments, chemosymbiotic lucinid bivalves [8,9]. Although algae and to a lesser extent seagrasses release particulate and dissolved organic matter into the water [7,10,11], the planktonic organisms that depend on these sources of nutrition exist in low abundance, with the result that suspension-feeders tend to be small except for semi-infaunal bivalves that extend above the plant cover in mesotrophic grassbeds [8,12,13]. This oceanic regime prevails in situations where most nutrients are generated, retained and recycled on the seafloor as on atolls, offshore reefs, high limestone islands and seagrass meadows in carbonate-dominated sediments [5,14]. With higher rates of nutrient input from rivers or upwelling, there is a shift in primary producers towards faster-growing fleshy algae and, at the highest levels of fertility, dominance by phytoplankton [5–7]. In this more continental regime, suspension-feeders are abundant and often large, especially where plant cover is reduced [6,14]. Herbivores reach large sizes where benthic algal cover is high. Predatory gastropods can be large under either regime as long as large prey are available. In the tropics, oceanic and continental benthic communities support a separate cast of species, which thus appear to be specialized to one or the other trophic regime [8,15–18].

When applied to the fossil record, these relationships can be used to infer the relative importance of benthic and planktonic primary production and ancient tropical shallow-water marine ecosystems. To that end, I compiled data on maximum adult body sizes (expressed as shell lengths) of the largest species in each of 23 molluscan trophic guilds spanning the interval from the Eocene epoch of the Palaeogene period to the Late Neogene period, including the Recent.

2. Material and methods

I collected data on maximum adult size (largest linear dimension of shell in millimetres) in 23 guilds representing herbivores, suspension-feeders, chemosymbiotic bivalves, and predatory gastropods in shallow-water marine ecosystems of the euphotic zone. A linear dimension was chosen because it is the most direct measure of body mass available and because it correlates highly with other, more precise estimates of mass [19]. Within a guild, species have similar shapes, so that artefacts arising from differences in geometry are minimized. Inferences of diet and mode of life were made from the known habits of living relatives and other considerations based on sedimentology and functional morphology. Data were obtained from Recent and fossil collections including those at Museum Naturalis (Leiden), Palaeontological Research Institute (Ithaca, NY), California Academy of Sciences (San Francisco), US National Museum of Natural History (Washington), and the author. Additional data were taken from the taxonomic and ecological literature. I excluded guilds whose members are known or suspected to bear photosymbionts (cardiid bivalves) as well as bivalves with chambered shells (Spondylidae and Ostreoidea), whose chambers may indicate bacterially aided calcification and growth. Among consumers of benthic photosynthesizing organisms, species that feed on corals, sponges and other animal–plant symbiotic partnerships were also excluded, because none of these species reaches the sizes of species that feed on algae or seagrasses.

3. Results and discussion

During the Eocene and Oligocene, the largest consumers were herbivores and chemosymbiotic lucinid bivalves (table 1, figure 1 and electronic supplementary material, table S1). The only conspicuously large suspension-feeders were slow-moving or sedentary turritellid gastropods, non-siphonate burrowing bivalves and one Late Eocene venerid (Venidia from Colombia). Other suspension-feeders, especially highly mobile scallops and burrowing bivalves, remained small. With the exception of the Late Eocene shell-enveloping volute Santeevoluta, no Eocene or Oligocene predatory gastropod exceeded a length of 170 mm.

Table 1.

Maximum body sizes of molluscs in tropical Cenozoic trophic guilds.

category	faunas (n)	size (mm)	taxon
herbivores
ampullinids
Eocene–Oligocene	7	215	Ampullinopsis
Miocene–Recent	6	50	Cernina
sand-dwelling neritids
Eocene	3	190	Velates
Recent	1	37	Linnerita
high-spired gastropods
Eocene–Oligocene	3	1000	Campanile
Miocene–Recent	7	105	Cerithium
cowries (Cypraeidae)
Eocene	5	300	Gisortia
Miocene–Recent	9	147	Cypraea
stromboideans
Eocene–Oligocene	5	180	Dilatilabrum
Miocene–Recent	9	400	Lobatus
chemosymbiotic lucinid bivalves
Eocene–Oligocene	3	311	Superlucina
Miocene–Recent	10	104	Anodontia
suspension-feeders
calyptraeid gastropods
Eocene–Oligocene	5	42	Crepidula
Miocene–Recent	7	66	Crucibulum
turritellid gastropods
Eocene–Oligocene	108	168	Turritella
Miocene–Recent	11	180	Turritella, Zaria
non-siphonate burrowing bivalves
Eocene–Oligocene	9	121	Crassatella
Miocene–Recent	11	145	Grandiarca
epifaunal byssate bivalves
Eocene–Oligocene	4	73	Cucullaearca
Miocene–Recent	7	160	Perna
venerid bivalves
Eocene–Oligocene	11	109	Venidia
Miocene–Recent	13	160	Mercenaria
scallops (pectinidae)
Eocene–Oligocene	3	53	Lyropecten
Miocene–Recent	10	200	Nodipecten
deep-burrowing gaping bivalves
Eocene–Oligocene	4	95	Panopea
Miocene–Recent	7	200	Pholadomya
razor clams
Eocene–Oligocene	4	58	Eosolen
Miocene–Recent	6	160	Solen
predators
drilling naticid gastropods
Eocene–Oligocene	7	40	Cepatia
Miocene–Recent	11	91	Glossaulax
echinoderm-feeding cassid gastropods
Eocene–Oligocene	5	87	Galeodea
Miocene–Recent	7	400	Cassis
drilling muricid gastropods
Eocene–Oligocene	12	163	Clavellofusus
Miocene–Recent	11	600	Triplofusus
melongenid gastropods
Eocene–Oligocene	8	115	Lacinia
Miocene–Recent	9	330	Hemifusus
prey-enveloping volutes
Eocene–Oligocene	2	225	Santeevoluta
Miocene–Recent	6	468	Melo
vasid gastropods
Eocene–Oligocene	2	68	Eovasum
Miocene–Recent	9	149	Vasum
worm-eating turbinellid gastropods
Eocene–Oligocene	4	149	Turbinella
Miocene–Recent	7	910	Syrinx
worm-eating Conus
Eocene–Oligocene	4	98	C. tortilis
Miocene–Recent	9	212	C. prometheus

Figure 1.

Global trends in maximum body size in representative tropical molluscan clades. Open squares, herbivore cowries; filled triangles, chemosymbiotic lucinids; open circles, suspension-feeding venerid bivalves; filled squares, predatory whelks.

Maximum body size increased after the Oligocene in all eight guilds of suspension-feeders (mean factor of increase from largest Eocene to largest Pliocene to Recent species 2.3 ± 1.0, range 1.2–4.2; figure 1). This trend is significant at or below the p = 0.05 level in all guilds except non-siphonate burrowing bivalves, and is most pronounced in epifaunal bivalves and highly mobile burrowers. Post-Oligocene increases in maximum body size are also significant in stromboidean herbivores (factor of increase 2.2) and in all nine predatory guilds (mean factor 4.0 ± 2.4, range 2.1–10.1). Among the 18 guilds showing a size increase over time, 13 had exceeded Eocene and Oligocene maximum sizes by the Early Miocene, two did so by the Early Pliocene, and the remaining two reached this status in the Recent fauna (electronic supplementary material, table S1). Pliocene to Recent maximum sizes exceed those of the Early Miocene by a factor of 1.3 or more in 14 guilds but do not rise above Early Miocene values in four others (turritellids, scallops, venerids and vasids). Trends of decreasing maximum body size are significant in lucinids (by a factor of 1.3 to the Pliocene and 3.0 to the Recent) and in the four non-stromboidean herbivorous guilds (mean factor of Post-Eocene decrease 5.4, range 2.1–10.1). Early Miocene sizes were still substantially higher than Recent ones in lucinids, ampullinids and high-spired herbivores (electronic supplementary material, table Sl). For the 21 guilds found throughout the tropics, these temporal patterns in maximum body size occurred in both the Atlantic–East Pacific and Indo–West Pacific (IWP) realms. The trends are therefore neither region nor taxon-specific (table 1 and electronic supplementary material, table S1). As a result of these changes, the largest Pliocene to Recent tropical shell-bearing molluscs other than oysters and photosymbiotic tridacnine giant clams (not considered here) are predators, followed successively by stromboideans, suspension-feeders, non-stromboidean herbivores and lucinids. The IWP realm is home to the largest living members of the four non-stromboidean herbivorous guilds (two of which, sand-dwelling neritids and ampullinids, are found nowhere else), four predatory guilds (muricids, melongenids, turbinellids and volutes), and epifaunal bivalves. Stromboideans, lucinids, venerids, deep-burrowing bivalves and four predatory guilds (cassids, whelks, vasids and worm-eating cones) reach maximum body sizes in the Atlantic; and naticids and four suspension-feeding guilds (calyptraeids, non-siphonate burrowing bivalves, scallops and razor clams) do so in the eastern Pacific (electronic supplementary material, table S1). Turritellids reach comparable maximum sizes in the IWP and eastern Pacific.

All Pliocene to Recent giant suspension-feeders and predatory naticids, whelks, melongenids, volutes, turbinellids, and cones occur exclusively near large land masses in planktonically productive settings. Large herbivores and predatory cassids, muricids and vasids occur in these settings as well but also extend to more oligotrophic environments on oceanic islands and in the Caribbean. The size distribution of large species in Recent carbonate-rich environments thus conforms to the Eocene pattern except that modern predators reach larger sizes. Carbonate-dominated habitats of the Early Miocene Chipola Formation of Florida and the Miocene limestones of Java and Borneo likewise support small suspension-feeders and relatively large herbivores and predators (electronic supplementary material, table Sl), conforming to the Eocene pattern.

Post-Pliocene decreases in maximum body size occurred in three guilds in the IWP (ampullinids, high-spired herbivores and lucinids) and in nine western Atlantic guilds (high-spired herbivores, cowries, calyptraeids, turritellids, non-siphonate burrowers, epifaunal byssate bivalves, scallops, melongenids and worm-eating cones); a tenth (ampullinids) became extinct there. These decreases reflect Pliocene and Early Pleistocene extinctions of large-bodied taxa and, in much of the western Atlantic, a decrease in planktonic and seagrass-generated productivity [20–25].

These trends are not correlated with, or artefacts of, changing diversity. Although the most diverse faunas might be expected to contain the largest Cenozoic species in a guild, this is generally not the case. The highest molluscan diversity in the Cenozoic is reached in the Middle and Late Eocene of France, the Late Oligocene of France and the Early Miocene of Florida. With the exception of very large herbivorous cowries and high-spired gastropods in the Middle Eocene of France, the other hyperdiverse faunas do not contain exceptionally large-bodied species. Indeed, body size of the largest species in all guilds increases from the Late Oligocene to the somewhat less-diverse Early Miocene in France (data not shown). In Florida, size increased among the largest species of guilds from the Early Miocene to the less-diverse Plio-Pleistocene in all guilds except vasids (electronic supplementary material, table S1).

The size distribution of large members of molluscan trophic guilds in shallow tropical seas during the Palaeogene parallels the pattern observed in Recent oligotrophic settings. I therefore interpret Eocene ecosystems to be characterized by low productivity in the plankton, as reflected by the small sizes of suspension-feeders (especially active ones), and by very high primary productivity on the seafloor, as indicated by gigantic herbivores and lucinids. These inferences are consistent with the widespread dominance of large photosymbiotic benthic Foraminifera and to a lesser extent corals on Eocene carbonate platforms [26], by the occurrence of highly productive and diverse seagrass meadows (reviewed in [27]), and by the appearance by Early Eocene time of herbivorous fishes and sirenians with high metabolic demands [28,29].

Low-nutrient flux from the land is likely to be the main cause of low planktonic and high benthic productivity during the Eocene. Most nutrients were generated and retained on the seafloor rather than in the water column. Turritellid gastropods were abundant and often large in carbonate-rich Eocene sediments, and must have required high-nutrient conditions as do their modern counterparts [30]; but it is possible that these level-bottom surface-dwellers gained much of their food from suspensions at the sediment–water interface and from the sediment itself. High-nutrient conditions in carbonate-rich environments are found in the tropics today only in the closed lagoons of atolls [14,30,31], where the dominant consumers are sedentary suspension-feeding bivalves and very small turritellids.

Other factors contributing to the Eocene pattern of tropical marine productivity include high temperatures at low to mid latitudes [32,33], permanent stratification of the water column (preventing nutrients from upwelling to the surface and fertilizing the plankton there), and sluggish ocean circulation [34,35]. Similar conditions prevailed during supergreenhouse intervals of the Late Cretaceous [36,37]. Brief episodes of enhanced weathering on land and greater abundance of plankton, brought on by sudden increases in carbon dioxide and temperature, occurred at the end of the Palaeocene and during the Eocene [38–41], but they may have been too short for benthic suspension-feeding species to capitalize on the planktonic enrichment through evolutionary size increases.

After the Oligocene, benthic productivity along continental shores remained high, but planktonic productivity rose sharply, as indicted by large increases in the maximum size of suspension-feeders throughout the continental tropics. The size trends in suspension-feeding molluscs parallel the origin and diversification of plankton-feeding procellariiform birds (petrels and their relatives) and mysticete whales [42–44] as well as balanomorph barnacles [45]. High water-column productivity especially from the Langhian (Middle Miocene) onwards, was made possible by more intense upwelling, more vigorous meridional ventilation of the ocean thanks to polar cooling and the narrowing of low-latitude ocean gateways, and especially by renewed intense global tectonic activity and consequent weathering of high-elevation terrains [46]. In Indonesia and mainland southeast Asia, extensive uplift and terrestrial runoff increased productivity beginning in the Late Miocene and especially in the Pliocene [47,48]. Ecosystems far from sources of land-derived nutrients remained oligotrophic despite the global intensification of ocean circulation and the high frequency of cyclones, which reduce stratification in the upper water column. As noted above, much of the Caribbean region shifted from a terrigenous to a carbonate sedimentary regime and became more oligotrophic, as reflected by the post-Pliocene decrease in the maximum size of most suspension-feeding guilds.

Besides the enabling factors controlling productivity, maximum sizes are affected by selection. My findings imply that selection in favour of large size was especially intense for predatory gastropods from the Miocene onwards, even in oligotrophic regions. This selection was most intense and yielded the largest species in conditions of high predictable planktonic productivity along continental coasts. It also led to the evolution of high-energy predatory methods that involve the application of force, as in shell-chipping and shell-wedging by several Neogene lineages of muricids and buccinoidean whelks, again along the productive shores of continents [49].

Data on offshore phytoplankton abundance and sea water chlorophyll content indicate that planktonic productivity in most open-ocean regions of the world has declined by an average of 1 per cent during the last century, and that oligotrophic waters have spread over the same period [50]. Climate models based on ocean circulation predict that these trends will accelerate during the next century [51]. A lower influx of minerals from mountainous terrains owing to the global damming of large rivers [52] may be contributing to these trends, even though concentrations of nutrients (phosphates and nitrates) in coastal waters are increasing because of agricultural and urban runoff [53,54]. Tropical marine ecosystems affected by reduced inputs of land-derived iron and silica and by rising temperatures may thus begin to approach Eocene patterns of primary production, in which benthic photosynthesizers dominate. It is important to monitor not only the planktonic productivity of near-shore ecosystems, but also the productivity, extent and composition of benthic primary producers on shores, reefs and seagrass meadows.