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Second, why are there so few

Primer transitions among the great realms?
Given the enormous challenges in
estimating speciation and extinction
Biodiversity in water rates, for most groups, it remains
15%

and on land unclear whether there are truly

differences in rates of diversification
across the three realms, and this
Richard K. Grosberg1,*, remains an area of very active
Geerat J. Vermeij2, research. Nevertheless, we can
and Peter C. Wainwright3 speculate on some of the major 85%
factors that collectively influence
Habitats in the sea, in freshwater, diversification.
and on land differ dramatically in
Current Biology
species composition and diversity. Amount of productive habitat
Of the roughly 1.5 million known As a general rule of thumb, high
species of macroscopic organisms biodiversity depends on high Figure 1. Diversity on land and in the sea.
on earth, the modern ocean — productivity over the long run (Figure The distribution of macroscopic species di-
despite its much larger area and 2A,B). There are exceptions, of versity in terrestrial (brown) versus marine
(blue) realms, according to May (1994).
volume — supports only about course, such as the highly diverse
15% of species, whereas terrestrial floras of southern Africa (Figure
environments account for about 2C) and western Australia where three physical realms of life and
80% of species, and freshwater terrestrial productivity is low, and how these patterns relate to the
for the remaining 5% (Figure 1). the diverse faunas of hydrothermal distribution of biodiversity.
Even when taking into account vents and the abyssal plain in
previously undetected biodiversity the deep sea. And in the world’s Habitat complexity
in all of the physical realms revealed oceans, there are notable areas in A three-dimensionally complex,
through molecular techniques, these temperate and polar waters that biologically constructed environment
differences appear to be robust — exhibit seasonally high productivity, is conducive to high diversity (Figure
certainly among multicellular but low diversity. Nevertheless, 2A,B). Much of the ocean comprises
organisms. deserts notwithstanding, terrestrial the relatively homogeneous
A closer look at these differences environments, for reasons that pelagic zone, which is inhabited
reveals two striking patterns: first, remain unclear, tend to be far by comparatively few macroscopic
it’s only relatively recently, in the more productive and cover a species. The shallow seafloor, by
last 100 million years or so, that larger relative area, than marine contrast, can be topographically
the number of species on land has ones. The most productive marine complex, because of vegetation
come to vastly exceed the diversity environments are confined to and reef-builders, including corals,
in the seas; second, despite hydrothermal vents and shallow- seaweeds, seagrasses, mussels, and
some transitions and overlaps in water, coastal zones, leaving much oysters, among others. Terrestrial
distribution, many major clades of of the pelagic zone and the deep sea environments are generally far more
plants, animals, fungi, and microbes relatively unproductive. Freshwaters physically complex, largely because
occur primarily in only one, or are generally shallower than the of habitat provided by plants,
two, of the three realms (Table 1). oceans, and many lakes and both above and below ground.
Although there are exceptions, rivers support high productivity of Moreover, physical gradients tend
particularly among fish and some either plankton or bottom-dwelling to be steeper, and extremes, for
decapod crustaceans (many crabs vegetation. instance of temperature, tend to be
and shrimp), this observation, The high productivity of greater in terrestrial environments.
together with abundant phylogenetic terrestrial environments is largely This, in turn, provides far more
and fossil evidence, implies that due to forests and grasslands habitat diversity over smaller spatial
evolutionary transitions among these and is, geologically speaking, scales than exists in most marine
realms are typically infrequent and a relatively new state of affairs. environments.
apparently difficult. Recent evidence from fossil leaves In contrast, the structural
These contrasts in diversity strongly indicates that during complexity of freshwater
continue to puzzle both ecologists the mid-Cretaceous (100 million environments is relatively low,
and evolutionary biologists, and years ago) there was a dramatic thanks to the short stature of most
possible explanations must span increase in terrestrial productivity, aquatic plants and the absence of
multiple spatial and temporal scales. as the land vegetation became reefs built by animals. (The absence
There are at least two fundamental dominated by flowering plants, of freshwater shrubs and trees, or
questions that must be answered: whose photosynthetic capacity far large algae, is in itself an intriguing
first, to what extent do the presently exceeded that of their predecessors. problem. Rooted freshwater plants
observed differences in diversity Nevertheless, it remains an tend to occur in clear, plankton-poor
reflect historical differences in rates important and open question how waters, whereas floating plants and
of diversification or biases in the present-day and historical levels phytoplankton dominate waters
rate of transitions between realms? of productivity differ across the of high productivity.) On the other
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Figure 2. Features of several major habitat types, and their association with species diversity.
(A) A new world tropical rainforest, typified by high primary productivity, high three-dimensional complexity, and high species diversity (photo:
Mary Plage, Getty Images). (B) A tropical coral reef, the marine equivalent of a tropical rainforest (photo: Mark Conlin, Getty Images). (C) The
fynbos, a relatively low productivity heathland limited to a coastal swath of the Western Cape region of South Africa, characterized by exception-
ally high plant diversity (photo: Richard I’Anson, Getty Images).

hand, freshwater environments are, feeding, which is almost unknown in their new surroundings. Not
by nature, more fragmented and thus on land, but very common in aquatic surprisingly, therefore, major
more island-like than most terrestrial environments because of the evolutionary groups of organisms
and marine environments, promoting medium’s higher density, may enable (i.e., clades) differ dramatically in
isolation and the potential for some internal brooders to capture the frequency of transitions between
diversification across smaller spatial dilute gametes. This, along with realms. For example, at least ten
scales. extended sperm storage, potentially independent lineages of mammals
allows at least some populations of (including six with exclusively
Physical differences in the media aquatic sessile species to persist at fossil species) have colonized
Water and air differ in viscosity, lower densities than might otherwise marine environments from the land,
density, specific heat, diffusibility be possible. sometimes by way of freshwater
of gases, concentrations of oxygen This effect notwithstanding, visual (e.g., cetaceans); whereas no
and carbon dioxide, conductivity, and chemical signals involved terrestrial gastropods, crustaceans,
and transparency. Beyond this, in mate location and recognition hymenopteran insects, or non-
seawater and freshwater also will typically operate over shorter angiosperm vascular plants have
differ in salinity, gas concentration, distances in water than in air, become marine.
density, and viscosity. All of these acoustic signals being a notable Cephalopods, echinoderms,
differences are temperature- exception. Thus, insofar as sexual tunicates, brachiopods, anthozoans,
dependent, and all have significant selection reduces genetic barriers to and hexactinellid (glass) sponges
biological consequences that speciation, terrestrial environments have remained exclusively marine
must affect both ecological and should on the whole be more throughout their long evolutionary
evolutionary processes. conducive to both the formation history; and only one or two clades
For example, although the per- and maintenance of species. Over of demosponges have colonized
distance energy outlay of swimming the last 100 million years, from freshwater (Table 1). Gastropods
in water at normal speeds is less mid-Cretaceous time onward, have made this transition in 33
than the outlay for running on land, sexual selection and other factors to 38 independent lineages, and
attainable speeds and agility are permitting rarity have allowed bivalves have done so in at least
substantially higher on land and in diversity to rise faster on land than 20 clades. The only groups in
the air, permitting smaller animals in the sea, especially among such which the reverse transition, from
to move greater distances at higher very diverse clades as flowering freshwater to the sea, has been
speeds when living out of water. As plants, fungi and insects, despite at all common are insects and
a result, animal-mediated gamete huge radiations among marine especially fishes. Teleost fishes have
transfer (including pollination) and molluscs, crustaceans and fishes. moved many times from marine to
propagule dispersal are widespread freshwater habitats, and the reverse,
in terrestrial environments but are Transitions between domains sometimes spurring significant new
rare in aquatic ones, especially in These three factors — productivity, radiations. Among angiosperms,
the sea. habitat complexity, and the physical only five lineages have become truly
Higher locomotor performance, properties of the media — may also marine, although the arrival of these
faster diffusion of chemical signals, limit the capacity of established plants in coastal marine settings
and more effective transmission taxa to make transitions from one has had profound ecological
of visual signals in air imply that realm to another. The evolutionary consequences beginning eighty
species attracting or choosing challenges and opportunities million years ago.
among mates at a distance can associated with such transitions In nearly all cases that have
maintain populations at much lower reflect the adaptability and potential been investigated phylogenetically,
densities than in liquid media. performance levels of individuals, secondarily marine lineages
Nevertheless, active suspension as organisms compete for resources with freshwater ancestors have
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Table 1. Distribution of biodiversity among the three major physical realms of life.

Taxon Marine Freshwater Terrestrial

Sponges 9,000+ 200–250 0

Cnidarians 10,000 <50 0
Bryozoans 5–10,000 <100 0
Mollusks (Gastropods) 50,000 4–5,000 25–30,000
Mollusks (Bivalves) 11,000 1,400+ 0
Mollusks (Cephalopods) 800 0 0
Nematodes 35,000 2,000+ 106(?)
Arthropods (Insects) 1,400 (includes intertidal) 100,000+ 5–9 x 106
Arthropods (Arachnids) 1–2,000 5,000 (mostly mites) 106+
Arthropods (Crustaceans) 65,000+ 12,000 4–5,000
Platyhelminthes 15–20,000 1,000 300–500
Annelids (Polychaetes) 9,000 500+ 0
Annelids (Oligochaetes) <500 1,000+ 100
Echinoderms 6–7,000 0 0
Chordates (Mammals) 125 100+ 5,000
Chordates (Fish) 15,000 15,000 0
Chordates (Other vertebrates: <500 (excluding birds) 7,000+ <20,000
Amphibians, crocodiles, lizards,
snakes, turtles, birds)
Chordates (Tunicates) 3,000 0 0
Fungi <1,000 <1,000 106++(?)
Plants (vascular macrophytes) <100 2,500+ 250,000+
Plants (other macrophytes) 10,000 <500 30,000+ (including mosses)

Rough estimates of species diversity, synthesized from multiple sources, in major groups of multicellular, macroscopic organisms, across marine,
freshwater, and terrestrial realms. To the extent possible, we assigned organisms to habitat according to where they breed or spend the majority of their
life.

undergone very little diversification groups are osmotically highly in lakes as well as on reefs. Progress
in the sea. Vermeij and Dudley adaptable and move easily between in understanding such transitions
(2000) estimated that there are some fresh and salt water. Moreover, all must come from studies of how
1400 insect species that could be fossil ray-finned fishes from this agencies of evolutionary change
considered marine, representing well period are from marine deposits. interact with the physical properties
over 100 separate invasions. Like Finally, even if marine fishes did of different media as modified by the
secondarily marine spiders, mites, indeed evolve from freshwater species that already occupy target
scorpions, millipedes, centipedes ancestors, they would be the only environments.
and land plants, marine insects major group of organisms that This problem is especially
have undergone little speciation attained comparable diversity in the daunting for microbes, whose scale
compared to their terrestrial sea as in the habitats from whence of interaction is tiny compared to
relatives. Even in marine mammals, they came. the world of multicellular organisms.
only four marine clades (cetaceans, The evolutionary fates of clades For instance, there may be as many
sirenian sea cows, pinniped seals, making transitions among the great as 20,000 ‘species’ of microbes
and fossil desmostylians) underwent realms depends on the inherent in a liter of seawater. As with all
substantial adaptive radiation. adaptability of their physiological organisms, scaling such samples
A singular exception to this and developmental systems, as up to global estimates of diversity
pattern has recently been claimed well as on the ability of incumbents remains a major challenge. At this
for fishes. In a phylogenetically to exclude competitors that are point, however, sampling is far
informed analysis of living species initially poorly adapted to the new too limited, and we know far too
of actinopterygian (ray-finned) medium. In its new surroundings, little about diversity, distribution,
fishes, Carrete Vega and Wiens a clade may diversify, the extent dispersibility, and speciation of
(2012) infer that existing marine and ease of which depend on unicellular organisms to predict
clades are derived from freshwater dispersibility and the role of sexual whether the patterns of transition
ancestors, and notably, the number selection and other processes and diversification across physical
of freshwater species is nearly that cause populations to become realms evident in multicellular
equal to the diversity in the sea. genetically isolated from one organisms apply to microbes.
Rates of diversification were another. Like vertebrates in general, The contrasts we highlight
estimated to be about the same in fishes, because of their enhanced here show that, although major
freshwater and marine environments, homeostatic capacity, seem far more principles of ecological organization
including reefs. There are reasons likely to cross ecological hurdles cut across systems inhabiting
to be skeptical of some of these between fresh and salt water than different media, differences in the
inferences. For one, ancestral most other organisms, and sexual physical properties of the media,
habitats of fishes are particularly selection has been a conspicuous the steepness of environmental
difficult to reconstruct; many fish driver of speciation of many groups gradients, and the relationship
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between the geographic distribution placed cashew nuts where the pebble
of favorable habitats and Correspondences had been, in 10 trials over three days.
dispersibility nonetheless greatly Testing took place in visual isolation
influence how species interact with from the group, but (to avoid the
each other, how and to what extent Spontaneous stress of isolation) in the company of
speciation occurs, and the kinds of
adaptations that are likely to evolve.
innovation in tool Heidi, a submissive female.
In the first test, after trying an
Biodiversity is more than counting manufacture and undersized stick from the aviary’s
species; it is about understanding floor, Figaro started breaking a large
interactions, phenotypes, and use in a Goffin’s splinter off the beam (European
evolutionary processes in a
heterogeneous biosphere. cockatoo larch, which had previously been
left untouched by the animals),
using his beak through the wire
Acknowledgments
Alice M.I. Auersperg1, Birgit Szabo1, mesh. Heidi joined in for the last
We thank Mark Denny, Matt Friedman, Auguste M.P. von Bayern2,3, cut, but Figaro chased her away and
Stephanie Kamel, Tom Schoener, and Richard and Alex Kacelnik2 finally got hold of the splinter by
Strathmann for many useful discussions threading it in through the mesh. He
and insightful comments. Grants from the Accounts of complex tool innovations immediately started to use it to rake
US National Science Foundation (OCE 09- in animals, particularly in species not in the nut. Occasionally the nut fell
29057 to R.K.G. and DEB 10-61981 to P.C.W.) adaptively specialized for doing so, off the distal side of the beam, and
supported this work. are exceedingly rare and often linked we repositioned it. The curved bill
to advanced cognitive abilities in the forced the bird to work diagonally
physical domain [1], even though the downwards to see the movement of
Further reading
Benton, M.J. (2001). Biodiversity on land and in
relation between such capabilities the reward (see Supplemental Movie
the sea. Geol. J. 36, 211–230. and intelligence is poorly understood S1). Figaro combined straight pulls
Boyce, C.K., and Zwieniecki, M.A. (2012). Leaf [2]. For this reason, discoveries (placing the tool’s end behind the
fossil record suggests limited influence of
atmospheric CO2 on terrestrial productivity of such capabilities transcend nut and pulling it towards him) and
prior to angiosperm evolution. Proc. Natl. anecdotal value and contribute sideward levering movements against
Acad. Sci. USA 109, 10403–10408. significantly to comparative cognition the grid. He used 10 tools in 10 trials,
Carrete Vega, G., and Wiens J.J, (2012). Why are
there so few fish in the sea? Proc. Roy. Soc. B [3–5]. Among birds, there are several nine of which were manufactured and
279, 2323–2329. reports of tool innovations in corvids, one ready-made (Figure 1A).
Denny, M.W. (1993). Air and Water: The Biology but very few documented records Time for manufacture improved
and Physics of Life’s Media (Princeton:
Princeton University Press). in other families (for example across trials, indicative of learning,
Friedman, M. (2010). Explosive morphological [1,3–7]). Here, we report a case of but, notably, improvement was
diversification of spiny-finned teleost fishes spontaneous tool innovation in the not gradual: the first attempt took
in the aftermath of the end-Cretaceous
extinction. Proc. Roy. Soc. B 277, 1675–1683. Goffin’s cockatoo (Cacatua goffini), nearly 25 minutes, but afterwards
Logares, R., Brate, J., Bertilsson, S., Clasen, J.L., a species endemic to the Tanimbar the mean time for manufacture was
Shalchlian-Tabrizi, K., and Regefors, K. (2009). short and stable (excluding the first
archipelago in Indonesia. Like most
Infrequent marine-freshwater transitions in
the microbial world. Trends Microbiol. 17, corellas, they live in social groups test, X ± SE = 2:27±0:34; Figure
414–422. (~10–100) in tropical dry forests, 1B). Except for tool T6, which was
May, R.M. (1994). Biological diversity: differences
between land and sea. Phil. Trans. Roy. Soc.
roost in simple tree holes, and feed initially too long (Figaro halved it
Lond. B 343, 105–111. mainly on a seed based diet (which following one ineffective raking
Mora, C., Tittensor, D.P., Adl, S., Simpson, A.G.B., occasionally causes interference with attempt), the splinters were cut off
and Worm, B. (2011). How many species are
there on Earth and in the ocean? PLoS Biol.
agriculture) [8]. There are no records at their final, suitable length (Figure
9 e1001127. of tool-related behavior in the wild. S1 in the Supplemental Information).
Schmidt-Nielsen, K. (1972). Locomotion: energy We report how a captive male named T9 was a piece of bamboo from the
cost of swimming, flying, and running.
Science 177, 222–228.
Figaro successfully, reliably and aviary’s floor. T10’s manufacturing
Strathmann, R.R. (1990). Why life histories evolve repeatedly made and used stick-type was complex, involving four cuts to
differently in the sea. Am. Zool. 30, 197–207. tools to rake in food, manufacturing a branching twig on the aviary floor
Vermeij, G.J., and Dudley, R. (2000). Why are
there so few evolutionary transitions between
them from two different materials (Figure 1C). The first cut (cut 1) was
aquatic and terrestrial ecosystems? Biol. J. and displaying different steps and discarded; he then (cut 2) removed
Linn. Soc. 70, 541–554. techniques. a large side arm from near the twig’s
Vermeij, G.J. and Grosberg, R.K. (2010). The
great divergence: when did diversity on land During apparently playful stem by stepping on the stem whilst
exceed that in the sea? Integr. Comp. Biol. 50, explorations, Figaro inserted a stone twisting off the sidearm with his beak.
675–682. pebble through the aviary wire mesh, Figaro tried the entire side arm first,
where it fell on a structural wooden but after an unsuccessful insertion
1Department of Evolution and Ecology beam. After attempting to reach the attempt shortened the remaining first
University of California, Davis, One Shields pebble with his claw, he went away, by a third (cut 3) and finally cut the
Avenue, Davis, CA 95616, USA. 2Department fetched a piece of bamboo, returned, remaining part in half (cut 4). He used
of Geology, University of California, Davis, and used it to fish (unsuccessfully) for the resulting distal piece successfully
One Shields Avenue, Davis, CA 95616, USA.
3Department of Evolution and Ecology, the stone, adjusting the movement to retrieve the food.
University of California, Davis, One Shields of the functional tool-end to the We tested another male, Pipin, and
Avenue, Davis, CA 95616, USA. movement of the pebble. To follow Heidi in the same situation. Pipin
*E-mail: [email protected] this serendipitous observation we did not try to use tools, but Heidi,