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AN OVERGROWN quarry at East Kirkton near Edinburgh has yielded some
of the most remarkable fossil finds of recent years. Since 1984, Lizzie,
the oldest known reptile, and many other spectacular finds have turned up
there through the efforts of Stan Wood, a full-time fossil collector. One
special feature of the specimens from East Kirkton is their detail and age
– in particular they illuminate the time when scorpions colonised the land.

Scorpions once formed a prominent part of life on the land, yet very
little is known about how they left the sea. The East Kirkton specimens
show how these arthropods evolved to make the change. Some of the fossil
scorpions from this quarry are surprisingly large, adding fuel to the debate
about how big arthropods can be. The fossil record indicates that modern
scorpions, and presumably other arthropods (the group covering insects,
centipedes and crustaceans), that live on land, are small because of their
ecological role rather than any absolute mechanical or physiological limits
on their size.

East Kirkton Quarry is a site of international importance because it
fills a gap in knowledge of early life on land. More than 30 investigators
from a variety of disciplines are currently working on these rocks in a
project coordinated by Ian Rolfe at the Royal Museum of Scotland. By studying
the fossilised plants and animals of East Kirkton, and the environment in
which they lived, the team aims to reconstruct this ancient ecosystem.

At Manchester University, I have been looking at fossil scorpions, and
their ecology in particular, searching for clues to how arthropods might
have taken the great evolutionary step out of the water and onto the land.
Complete fossils of scorpions are rare. They have been found at only a handful
of sites, where unusual conditions preserved them . But fragments of their
cuticle, the organic exoskeleton that characterises arthropods, are common
in many ancient sedimentary rocks. Researchers recover these pieces by dissolving
the rock containing them using chemicals such as hydrofluoric and hydrochloric
acid. Often these fragments reveal details of the microscopic structure
of the exoskeleton, such as the lenses of compound eyes. When there are
enough pieces, palaeontologists can reconstruct the scorpions from which
they came.

These fragmentary remains have filled many gaps in the evolutionary
record, because they allow researchers to examine the evolution and habits
of the early scorpions in great detail. In particular, because organs such
as eyes and fragile sense hairs are usually very well preserved in these
specimens, we can follow the way in which sensory systems changed through
time. Information of this quality is particularly valuable for the story
it tells about how these extinct species lived, day by day. By piecing together
the various lines of evidence from complete fossils, fragments of cuticle,
and bonanzas such as the East Kirkton finds, we have built up a picture
of the complex history of the scorpions and their role in ancient ecosystems.

The earliest scorpions lived in the Silurian period, around 430 million
years ago, on the bottom of shallow tropical seas. These ancient forms look
superficially like modern scorpions, but because they lived in water, they
probably took in oxygen through gills which were concealed behind plates
of cuticle on the underside of their abdomens. These abdominal plates were
attached to the body wall only along their front edges, so that the scorpion
could flap them open and admit water into its gill chamber above. In contrast,
modern scorpions have four plates on the underside of their abdomens, joined
to the body wall all the way around their edges. These abdominal plates
cannot flap open. Instead, each plate, known as a sternite, is perforated
by a pair of holes, called stigmata, through which oxygen and carbon dioxide
diffuse. Above each hole is a chamber from which many thin membranous folds,
called lamellae, project into the scorpion’s body cavity. These lamellae
form the surface over which gaseous exchange occurs, as the lungs do for
humans, and are stacked together like the pages of a book; this earns them
the title of ‘book-lungs’.

Undersea predators

There are other differences between these early scorpions and modern
ones that live on land, principally in the way they feed and the structure
of their legs. Like other arachnids, modern scorpions are liquid feeders.
They take fragments of their prey into a cavity in front of their mouth,
the preoral cavity, and exude digestive juices onto the food. They then
suck back only the liquid mixture of digestive juices and partly digested
food through the mouth and into the gut. Liquid feeding is clearly not the
most efficient way for an aquatic organism to eat – just imagine trying
to eat a bowl of soup underwater. Not surprisingly, the Silurian scorpions,
which other evidence suggests lived in water, lack a preoral cavity, and
seem to have fed on solids.

Silurian scorpions were almost certainly predators. They have not only
the strong pincers and stinger characteristic of scorpions today, but also
a visual system ideally suited to active hunting. With a pair of eyes close
together right at the front of their heads, in a good position to give stereoscopic
vision, Silurian scorpions could judge the distance to their prey accurately.
In addition, they had two large compound eyes composed of as many as 1000
individual facets on each. This combination of eyes gave these ancient scorpions
a wide angle of vision.

Silurian scorpions have legs with the same number of segments as those
of modern species, but their structure differs. The relative proportions
of the different segments and the orientation of the various joints suggests
that they would not have been strong enough to function efficiently on land.
This type of leg was no problem in water, because the scorpions were buoyant.

By 400 million years ago, in early Devonian times, fragments of scorpion
start to turn up in sandstones that formed in rivers, a sure indicator that
by this time they had moved into freshwater habitats. The remarkable thing
about these fragments is that some of them came from scorpions a metre long,
which palaeontologists have endowed with evocative names such as Brontoscorpio.
The size of these scorpions might have enabled them to overcome some of
the physiological problems associated with the move from salt water to fresh
water.

Throughout the rest of the Devonian period, there are few scorpions
in the fossil record. Most of the evidence, from the type of rocks in which
they are preserved, suggests that at this time they were aquatic animals,
living in rivers, lakes and, in at least one case, a marine lagoon.

By far the greatest number of fossil scorpions have been recovered from
rocks between 320 and 290 million years old, the Upper Carboniferous period.
At this time large areas of Europe and North America were covered by low-lying
tropical forest. Many of the rocks formed at this time come from sediments
that accumulated in flood-basins, lakes and deltas, ideal for preserving
the remains of land animals. Upper Carboniferous scorpions look far more
like modern scorpions than their predecessors did. They all have a preoral
cavity, which had started to develop in some Devonian scorpions, and nearly
all species have legs that seem designed for life on land rather than in
water. But, because both structures could function as well in water as out,
neither proved conclusively that these scorpions lived on land.

Gills for water or lungs for land?

Only the structure of their respiratory organs can show unequivocally
whether these scorpions breathed water or air. So, did these Upper Carboniferous
scorpions have gills or book-lungs? This has always been the pivotal question,
and a difficult one to answer because the respiratory organs are so fragile
that they are rarely preserved as fossils. Palaeontologists have assumed
that the Carboniferous scorpions were aquatic because they have abdominal
plates like their Silurian ancestors, rather than the sternites with stigmata
of modern scorpions. But two new specimens from East Kirkton, 340 million
years old, have traces of their respiratory structures preserved above abdominal
plates – and they are true book-lungs rather than gills. Book-lungs, in
what in all other respects is a typical Carboniferous scorpion, confirm
what palaeontologists had suspected; most Carboniferous scorpions were really
terrestrial, as their way of feeding and the structure of their legs suggested
all along. Moreover, these early book-lungs appear to fall part way between
the book-lungs of modern scorpions and the book-like gills which the aquatic
scorpions possessed, and they offer some clues to how gills developed into
lungs. Although this is the only example of book-lungs in a scorpion of
this age or older, we can now wonder whether the older specimens, particularly
those from the late Devonian and early Carboniferous, were amphibious, or
even fully terrestrial. Perhaps scorpions have been land-dwellers for longer
than we imagined.

One surprise that comes out of East Kirkton quarry is that adult scorpions
were very large. The biggest complete scorpion found so far must have been
between 35 and 40 centimetres long, a giant by today’s standards. But fragments
from the quarry suggest that adults grew much bigger. One piece made up
of two segments of a tail and a stinger, which Wood found in a stone wall
near the quarry, belonged to a scorpion around 70 centimetres long. This
specimen and many hundreds of others from the site came from just a few
closely related species of terrestrial scorpions. There are enough fragments
of cuticle in sequences of sedimentary rocks to show that scorpions generally
grew smaller through the Carboniferous, so that by about 300 million years
ago adults were usually only 30 centimetres long.

No one really knows why the larger scorpions disappeared but the trend
is matched by changes in their sensory systems. In general, the visual system
became less important, and other senses improved. The eyes on the front
of the heads of aquatic scorpions gradually moved backwards. In some modern
types they now lie in the back half of the headshield. Over the same time,
the compound eyes at the sides gradually contained fewer and fewer separate
lenses. By Upper Carboniferous times (300 million years ago), most families
of scorpions had between 20 and 40 lenses in each eye, while some lost this
pair of eyes altogether. Modern scorpions have only between two and five
separate lenses on each side. These changes would have led to a loss of
resolution and poorer eyesight. But they were accompanied by improvements
in the way sense organs on the pincers and legs were organised, and by the
development of new sense organs such as long slender hairs specifically
adapted to pick up slight movements of air.

Nightlife in the Carboniferous

All these changes imply that, through the Carboniferous, scorpions were
turning to nocturnal activity, rather than hunting by day as their ancestors
had done. Against this background, the reduction in size can be seen as
a trend towards a different way of life, hiding away by day beneath vegetation
or in burrows. Scorpions 30 centimetres or more long are not particularly
suited to this mode of life. The giant Lower Carboniferous scorpions were
probably active by day, preying on other arthropods and small vertebrates.

During Carboniferous times, the vertebrates were also establishing themselves
on land, and as the East Kirkton finds show, some of the land-going amphibians
may have grown to 2 metres long. Before the vertebrates gained a firm foothold
on the land, scorpions were the most formidable predators there. But because
vertebrates have an internal skeleton, and so can grow to be much bigger
than arthropods on land, the predators eventually became prey; vertebrates
displaced scorpions as the dominant carnivores on land. The need to avoid
such predators seems the most likely reason why scorpions changed their
way of life.

But the existence of these big scorpions, living on land in the Carboniferous,
means that the maximum size of modern scorpions cannot be limited by absolute
mechanical constraints, such as the strength of their cuticle, or by limits
on their physiology like the efficiency of their respiratory or circulatory
systems .

Today, scorpions are notorious for their harmful stings rather than
their ecological significance. From what we know of modern scorpions we
certainly would not have guessed that their ancestors had such an eventful
evolutionary history. Palaeontologists are accustomed to thinking of evolution
in terms of morphological change. On these grounds scorpions have been extremely
conservative; they never achieved any great diversity, their form has changed
little through millions of years, and they never gave rise to any new groups
of arthropods.

What their history shows well is the way in which ecological roles of
organisms may evolve as the ecosystems they form part of undergo change.
Although they left the sea only a short time before the vertebrates, perhaps,
for a while, scorpions really did rule the land.

Andrew Jeram is a research fellow in the Geology Department of Manchester
University, currently investigating the earliest land animals.

* * *

1: East Kirkton’s recipe for preserving its ancient inhabitants

EAST KIRKTON Quarry has preserved unusually clear traces of life millions
of years ago. The sedimentary rocks there are dominated by an unusual limestone
which is made up of many thin layers. Thin bands of calcium carbonate alternate
with chert (fine-grained quartz) and clay to make a rock known as a laminated
limestone. Many of the bands are made of volcanic ash and debris, suggesting
that there were volcanoes nearby when the rocks formed.

The sediments were laid down under water, in a shallow freshwater lake
or lagoon, but the East Kirkton fossils came from communities living on
the vegetated slopes of volcanoes close to the lake and were occasionally
washed into the lake along with the volcanic ash. The limestone as a whole
contains plenty of fragments of charcoal which probably came from fires
set off by volcanic eruptions.

Some of the water in the lake came from hot springs associated with
the nearby volcanoes; minerals carried in the spring waters may have made
the lake uninhabitable. Its sediments contain no fossil fish, and very little
evidence of any other aquatic animals. The remains of land animals and plants
washed into the lagoon remained undisturbed because there were no scavengers.
As a bonus for palaeontologists, the lake waters were so rich in minerals
that they impregnated bones and plant tissues quickly giving rise to unusually
good preservation.

The fossils show that a variety of land-going amphibians, reptiles,
and scorpions lived among vegetation around the lake, dominated by seed
ferns. Millipedes, and the earliest known harvestman spider make up the
rest of the assemblage we have discovered so far. There are also some very
large eurypterids, extinct relatives of scorpions, but palaeontologists
are not certain whether these animals lived on land or in water.

Arthropods that lived on land are also rare as fossils because their
exoskeletons are made up entirely of organic molecules in most groups. This
decomposes easily with the help of bacteria and fungi. Modern scorpions
grow cuticle containing a unique layer not found in other living arthropods,
which is called the hyaline exocuticle. This is easy to pick out because
it fluoresces in ultraviolet light.

When they examine fossil cuticle with a scanning electron microscope,
palaeon tologists find that this layer is the part that is preserved. It
seems to be far more resistant to decay than its surrounding layers, or
the cuticles of other arthropods. As an example, a piece of fossil cuticle
from Carboniferous sediments in Yorkshire is only 12 thousandths of a millimetre
thick, yet it came from a scorpion 30 centimetres long. More than 70 per
cent of the original thickness of the cuticle has decomposed, leaving only
the thin hyaline exocuticle preserved. This may explain why the cuticle
of other arthropods, such as insects, which lack this special layer, is
rare in ancient rocks, while that of scorpions is common.

Another factor that makes these fossils special arises because many
arthropods that lived in water, such as trilobites and crustaceans, have
cuticle that was mineralised while the animal was alive. The animals built
their exoskeletons with minerals such as calcite as well as organic molecules.

Scavengers have less interest in these remains, and so they last longer
on the seafloor after the animal dies. These animals can be preserved in
the environment in which they lived. They stand a better chance of being
preserved and so have a more complete fossil record than creatures that
lived on land.

* * *

2: The arthropods’ limits to growth

THE EXTERNAL skeleton was a significant evolutionary breakthrough, contributing
immensely to the success of arthropods in water and on land. However, the
exoskeleton also has its drawbacks, not least that it poses physiological
problems which might limit the size arthropods can attain on land.

A good example of this is the way in which arthropods breathe. Because
of their rigid exoskeleton, breathing in and out, known as tidal ventilation,
is far more restricted for them than it is for vertebrates. Although they
can use some tidal ventilation, arthropods depend more upon diffusion and
convective mixing of gases to move oxygen into and around their respiratory
structures. These two physical processes work well when oxygen has to travel
only a very short distance. In larger bodies, only bulk movement of air
by tidal ventilation will transport enough oxygen for the animal’s requirements.
This is a particular problem for insects, since they depend on branching
complexes of air-filled tubes, the tracheal system, which supply tissues
with oxygen directly. By contrast, arachnids and vertebrates transfer oxygen
to their blood, which can then be pumped around the body.

The large fossil scorpions from East Kirkton have abdominal plates which
could be flapped open and closed. This would have allowed them to ventilate
their lungs with currents of turbulent air, more efficiently than modern
scorpions can.

In practice, the mechanical properties of arthropod cuticle may limit
the size of arthropods living on land before any of the physiological constraints
take effect. As arthropods become bigger, they gain weight faster than the
strength of their cuticle increases. Once they exceed a certain size, the
exoskeleton can no longer support the weight of their body. It is quite
likely that the giant Carboniferous scorpions were approaching this theoretical
size limit.