You are on page 1of 18

Biogeography of Kemp’s Ridley Sea Turtles.

Badal Landge

Course: ENVR 4060 by Dr. Erin McCance and Mr. Robert Wheeldon

This Photo by Unknown Author is licensed under CC BY-SA


Historical Biogeography

Study conducted by the University of Alabama on sea turtle’s origin led to discovering

various 80-million-year-old fossils (Gentry, 2016). Most of these sea turtle fossils belong to the

ancient lineage of sea turtles from which modern species of sea turtles arise. The research

published in the Journal of Systemic Palaeontology states that fossils discovered were belonging

to the genus Ctenochelys acris, which comprised of sea turtles adapted to the shallow, sub-

tropical marine environment (Gentry, 2016). This fossil was found during the cretaceous period,

a period which was the last part of the Mesozoic era. The cretaceous period has seen diversity

magnify amongst sea turtles, with fossils from the cretaceous period showing variety in

physiological aspects and better adaptivity to predators with structural changes in carapace and

plastrons (Gentry, 2016). The cretaceous period lasted for approximately 79 million years

(Stacey, 2016). The kemp’s ridley sea turtles are a fairly new species of sea turtles, but their

ancestors have survived the minor extinction event 145.5 million years ago at the end of the

Jurassic period and also survived the extinction which took place in the Cretaceous-Paleogene

period (Wilson, 2001). Drew Gentry from University of Alabama states that climatic warming

during the middle segment of the Cretaceous period led to increase in temperatures and sea level,

thus providing an ideal niche for sea turtles to invade into. C. acris fossil documentation provides

strong evidence on the speculation that sea turtles were land based and originated from fresh

water ecosystems (Gentry, 2016). Sea turtles are speculated as land based reptiles before the

Jurassic period, but adapted themselves to a marine and deep warm water ocean during the

Mesozoic era or even prior to it (Gentry, 2016). Another speculation was turned to fact with

respect to which hemisphere had more sea turtle abundance during the Mesozoic era. Studying

the extinct sea turtle’s distribution and modern-day sea turtle’s distribution and comparing their
physiological traits to C. acris, it is discovered that they should have originated from the deep

south. When the C. acris physiology is studied, it strongly resembles the movements of snapping

turtles such as powerful hind limbs to push through water, and earliest sea turtles can be

compared to a giant-sized snapping sea turtle which later evolved into the bottom dwelling sea

turtle such as a Kemp’s ridley sea turtle. The study of origins and evolution of sea turtles provide

an important view into how past climates and environments shaped the behaviour of kemp’s

ridley sea turtles. It gives us an insight into the organism’s adaptability with respect to several

ecosystems throughout the history of the planet. Kemp’s ridley sea turtles may be a relatively

new species and a sister species of the most abundant olive ridley sea turtles, but their lineage

dates back to before more than 200 million years ago, making them one of few surviving

organisms throughout major extinction events (Reaves, 2012). One of the major extinction event

survived by kemp’s ridley and olive ridley sea turtle’s ancestors were the K-Pg extinction event

which was during the boundary between Cretaceous period and the Paleogene period. Geologists

in 1979 studying layers of rocks found fine line of grey layer between rocks dating to Cretaceous

period and Paleogene period (Robertson, 2013). This pattern was found in various locations all

over the world, inferred as a major extinction event took place between this transition of periods.

Further tests done stated that the grey rock particles comprised of high concentrations of iridium,

a rare earth element, but found in abundance amongst meteorites (Robertson, 2013). Another

data showed the formation of tiny glass like globes which are called tektites (Robertson, 2013).

Tektites are only formed when an extra-terrestrial object collides the planet with extraordinary

force. This data leads to our belief of a meteorite strike causing a major world-wide catastrophe

which caused the major extinction event at the end of the Cretaceous period and at the end of the

Mesozoic era (Robertson, 2013). The shockwaves generated by the collision resulted in high
global temperatures, hot boiling water tsunamis which cooked large mammals who couldn’t find

shelter alive. Here is where, sea turtles found safe shelter under water in deep waters in the

southern hemisphere. Gentry states that sea turtles invaded new niches with suitable sea levels

and temperatures during and after this period. Hence, by these facts we understand that the sea

turtles came to North America during this search and invasion movement by sea turtles after the

effects of meteorite would have been deteriorated. Post Mesozoic we see a brief period of

nuclear winter formed by combined effects of volcanic eruptions from India joining Asian

continent and result of meteorite collision. Several land based turtles were said to feed on

carcasses of large mammals and dead dinosaurs before moving into the ocean for increased

survivability and more availability of food and shelter (Robertson, 2013).

The image from study by Luis Alvarez illustrated the grey line which depicts the period known

as ‘Nuclear Winter’ caused by volcanic ash covering the entire planet.


Population Distribution of Kemp’s ridley sea turtle:

We have now established that the origins of sea turtles have been in the deep south before

migrating northward. Kemp’s ridley sea turtles have a complicated past with migrating

northwards. It is very unique that kemp’s ridley sea turtles are only found in the Atlantic coast of

the North American continent, mainly near the Gulf of Mexico and some kilometers of Florida

shoreline (Reaves, 2012). There are several geographic changes which took place over the years,

most importantly the rise and fall of sea levels (Bowen, 1991) and rise of land mass in the region

surrounding the Gulf of Mexico. Rise of the isthmus of panama led to series of changes in the

manner Kemp’s ridley distributed themselves (Bowen, 1991). At the first we have the much-

debated separation of Kemp’s ridley sea turtles from their sister species, the Olive ridley sea

turtles. The migration along to land mass changes must have separated the Kemp’s and Olive

ridley seat turtles (Bowen, 1991). With less data available to back most speculations, it is not

sure as to why species of the same genus behave so differently and have such drastic habitat

choices differences. It could also be due to the fact the Olive ridleys migrated into ocean before

the Kemp’s ridley. The current day distribution for the juveniles have been reportedly found in

the northern segment of the Gulf of Mexico, between Texas and Florida and sometimes go as far

as Nova Scotia in Canada (Reaves, 2012). Distribution of juveniles also depend on when and

where the Kemp’s ridley sea turtles set up their arribadas and is mostly dependant on presence of

predators and how long they last against rapid changing temperature (Reaves, 2012). The

juveniles who survive drift and latch onto the eastern Gulf Loop current and are carried by

Florida ocean current upwards and east. On occasions there have been reports of juvenile

Kemp’s ridley being found at the shores of Ireland. But Kemp’s ridley never nest at the shores of

Nova Scotia or Ireland, most return to their place of birth for nest as it is deemed the safest place
in their living memory (Reaves, 2012). Explanation of such behaviour is difficult, but we can

describe it as primitive organism’s behaviour. Such behaviour is seen is several sea turtles and

land turtles.

The habitat of the Kemp’s ridley sea turtles are shallow waters, where the range less than

165 feet depth is a suitable habitat for both adults and young Kemp’s ridley sea turtles. This

depth is suitable for finding adequate prey and camouflage with the surroundings to avoid being

preyed upon (Reaves, 2012). Juveniles float of the surface water and drift to a suitable niche.

Some juveniles float for months on floating marine vegetation and accumulated debris. These

patterns of movement are called drift lines and are taken up by several other sea turtles. There is

no knowledge as to what they feed on during this period, how far they drift, and how they make

it back to the shore (Reaves, 2012). There are several nesting sites or arribadas but a few major

ones. The largest one is in Rancho Nuevo in Mexico is the primary land habitat used for nesting.

In this major joint event Kemp’s ridley turtles bury holes in the sand and lay their eggs within.

Most nesting occurs in this stretch of Mexican beach. There are not any other known beaches

which hold so many nesting Kemp’s ridley turtles (Reaves, 2012).


Ecological Biogeography

In Texas coastal lines, marine ecologists have reported that Kemp’s ridley sea turtle and

the Loggerhead sea turtles separate their food resources without any conflict (Reaves, 2012). The

Kemp’s ridley feed on fast blue and spotted crabs, where as the Loggerhead sea turtles feed on

seapens and slow-moving crabs (Reaves, 2012). The Kemp’s ridley are also seen in a mutualistic

relationship with corals and sea vegetation, where Kemp’s control the population of crustaceans

which feed on the corals and corals serve as a perfect platform for juvenile Kemp’s ridley sea

turtles to start a safer life at sea, providing higher evasiveness from predators and abundant

availabity of food. The diet of both juvenile and adult Kemp’s ridley turtles comprise of crabs,

shrimp, snails, sea urchins, jelyfish, sea stars, small fish and occasionally marine plants (Reaves,

2012). Blue crabs are the primary preferred food choice, but scarcity can lead to Kemp’s ridley

opting for other marine organisms on the ocean floor (Reaves, 2012). Feeding habits of juveniles

is difficult to keep a check on, but dead carcasses have show shrimps, marine vegetation or any

floating animal matter located in the region of Gulf of Mexico or at the boundary of the Atlantic

ocean (Reaves, 2012). Kemp’s ridley sea turrtles don’t go far from the shore, unless they get

caught up into the ocean currents, which may take them far up north towards Europe or

somewhere in the mediterranean sea (Reaves, 2012). Reproductive behaviour of the kemp’s

ridley sea turtles is different from other sea turtles. The Kemp’s ridley come to the nesting sites

is large masses, and this is termed as arribada or the arrival in spanish. Over a period of several

hours or days the female Kemp’s ridley sea turtles simulataneously come to the waters near the

shore and lay eggs underground. This process normally takes place during the day, unlike other

sea turtles nesting which takes place at night. The nesting takes place on a single stretch of the

beach, indicating they nest together for a reason and it is not completely at random (Bernardo et
al, 2007). This process takes place every year with Kemp’s ridleysea turtle females nesting every

1 to 3 years, and average atleast one nesting every 2 years unlike other sea turtles who nest every

2 to 3 years (Lutz et al, 2002). The reason for arribada nesting could be many reasons, but none

have a scientific evidence backing it, due to the fact that it occurs only one or twice a year and

only in a very few places. Speculations can be made that this behaviour is to reduce the chances

of predation and high numbers of turtles will potentially scare of predators. The eggs are burried

in the sand and left for incubation. This is a major behavioural trait that tells us how Kemp’s

ridley behaved during the periods where earth was covered with volcanic ash and meteorite

nuclear sediments. The eggs must be burried to protect from predators, and the volcanic clouds

which covered the atmosphere. The Earth’s ground temperature remains almost constant during

the day and cools during the night. The incubation temperature underground is suitable for

Kemp’s ridley zygote to survive. Having a sea shore as is nesting site is also an ideal choice by

Kemp’s ridley due to the fact that sea shores have a humid climate and less variating

temperatures. This helps eliminate their limiting factor: Tempertature.

Limiting Factor: Temperature

Temperature plays the most important role in a Kemp’s ridley sea turtle’s life. It usually

occupys waters with warm water currents in between the two two tropical latitudes.

Temperatures between the tropic of cancer and tropic of capricorn are the most suitable for

Kemp’s ridley sea turtles, with the lowest possible temperture report for a Kemp’s to survive was

10 degrees celcius and the maximun threshold of temperature Kemp’s ridely can survive is 35

degree celcius (Lutz et al, 2002). Coincidently, the 35 degrees celcius threshold for survival also

applys to most plants in the tropics, with photosysthesis seizing at temperatures above 35 degrees

celcius, and the plant dying at 40 degree celius and over (Lutz et al, 2002). The role of
temperature in the determination of the Kemp’s ridley sea turtle’s gender is phenomenal. Over

the course of Kemp’s ridley’s population dynamics throughout history, we can only estimate

based of the surrounding environment what the populations of Kemp’s ridley would have been

like. With every era and temperature change, from high tempeatures extinction events to the

closest ice age at the late holocene era between 9300 BC to 10800 BC (Lutz et al, 2002). During

these times Kemp’s population must have changed drastically in terms of gender abundance.

This is due to Kemp’s zygotes hatching based on temperature. Below temperature of 29.5 degree

celcius, Kemp’s ridley sea turtles are born all males and above the temperatures of 29.5 degree

celcius, all females are born ( ). So we can assume that during the ice age, there must have been

gradual decrease in populations of Kemp’s ridley sea turtles, due to most of them being born

males, there would be less females nesting, leading to lowering in populations (Reaves, 2012).

Ecological interactions:

In the breeding season the female's Kemp's ridleys move towards the nesting beach, where in the

nearby waters, male Kemp's ridleys are already present year long. Breeding and courtship takes

place at the shores. The nesting period lasts from April, May to June, but on occasions it can

stretch out till August (Bernardo et al, 2007). Late nesting means that the year had a longer

winter and cooler spring season. The reproductive behavior of the Kemp's ridley is also based on

temperature and weather conditions throughout the year. The nest has a distinctive feature, it

takes the shape of an elevated dune, a few feet above the sea level (Bernardo et al, 2007). The

female then uses its fore limbs and beak like mouth to dig a hole in the sand. The eggs are laid in

the hole, which takes about 45 minutes. The Female Kemp's ridley is vulnerable from predators

during this period (Bernardo et al, 2007). Hence, the arribada nesting behavior is so important

amongst the Kemp's ridley sea turtles. In one egg deposit period, a female Kemp's ridley will
hatch between 90 to 100 soft-white eggs (Bernardo et al, 2007). The eggshells are made of

leathery coating and contain fluid covering on the surface. The incubation period lasts for 45 to

55 days based on weather conditions and temperature (Bernardo et al, 2007). The gender

determination based on temperatures takes place when Kemp's ridley are in their late embryo

form. The hatchings are hard-wired to make it to the sea as quick as possible (Bernardo et al,

2007). They also at a 100 percent success rate move only towards the nearest body i.e the the

Gulf of Mexico. This could be due to their genetic behaviour to evade predators as quick as

possible. Despite this behaviour, Kemp's ridley have been succumbed to predation and poaching

and only a few actually survive to sexually mature (Bernardo et al, 2007). It is widely accepted

fact that the juveniles may remember or imprint on the smell, chemical make up and magnetic

location of the place of their birth and return to the same place upon sexual maturity. Kemp's

ridley require 10 to 20 years to sexually mature, but after almost 2 decades the Kemp's ridley

return to their place of birth for mating and nesting purposes (Bernardo et al, 2007 ).

This Photo by Unknown Author is


licensed under CC BY-SA Arribada
Nesting occurs during the day time
unlike other sea turtles nesting.

This Photo by Unknown Author is


licensed under CC BY
Soft white eggs in a clutch
formation laid by Kemp’s ridley sea
turtle
Biological biogeography

The name of the turtles were coined by Richard Moore Kemp, who was the first to study

the specimen, but the origin of the name ridley is unknown. The scientific name of Kemp's ridley

sea turtle is lepidochelys kempii. It is a critically endangered species of marine organisms

distributed only in the North American coast along the Atlantic ocean (Reaves, 2012). On

attaining maturity, the Kemp's ridley sea turtles measure a 55 to 70 cm in length and weigh upto

35 to 45 kilograms. Compared to other sea turtles, Kemp's ridley is the smallest in size (Reaves,

2012). Its body is adapted to swimming in shallow waters by having a flipping motion of

swimming and front limbs are structured as flippers (Gentry, 2016). The Hind limbs work as

rudder to move through water. This is an important adaptation of the Kemp's ridley and shows its

evolution from its ancestor C. acris who moved through water like a giant sized snapping turtle

(Gentry, 2016). The shape of the carapace is oval and has a depressed dorso-ventral body

(Dundee, 1992). The carapace is connected to the plastron with bridges on both sides. The

bridges contain five pairs of costal scutes and each bridge qill carry 4 infra-marginal scutes

(Dundee, 1992). These infra-marginal scutes have been perforated by a deep pore, whose

opening leads to a gland. the glandular secretion from this pore opening has unknown functions,

but speculations have been made that the secretion functions in predator evasiveness, mapping

and location or a part of their sexual behaviour (Bernardo et al, 2007). Another major adaptation

of the Kemp's ridley is that their mouths have a beak like structure which has been developed to

feed of crustaceans (Reaves, 2012). As Kemp's ridley is a shallow water benthic feeder, the

require for a strong beaked mouth is necessary to feed on crabs, dig holes on ocean floors to

blend in with the surroundings, dig up marine vegetation, etc (Dundee, 1992 ). The beaked

mouth also has strong crushing surface which enhances its function (Dundee, 1992 ).
The juveniles Kemp's ridley sea turtles float of seaweeds and other marine vegetation.

Most recently they have been reportedly floating on human deposited debris. They also tend to

feed on the marine vegetation they float on following their drift lines (Reaves, 2012). The

carapace of juveniles Kemp's ridleys is dark purple to almost black (Dundee, 1992). They change

color as they mature to suit their surroundings. The mature Kemp's ridley take up neritic habitats

on the ocean floor, which is ranging from a depth of 50 ft to 165 ft deep (Bernardo et al, 2007).

The environment of the neritic habitat is filled with mineral deposits and marine vegetation. The

carapace of the mature Kemp's ridley sea turtles are greenish-gray in color and blends in

perfectly with the neritic habitat they reside in. The plastron's pale yellow color blends with

corals and marine vegetation (Reaves, 2012). There are several benefits of the camouflage.

Evasiveness from predators increases and chances of survival are increased. The ability to prey

upon crustaceans and small fish is also supported by their ability to blend in with the

environment (Gentry, 2016). Their preferred places of nesting such as dunes or swampy areas

also help them with camouflage. The eggs they hatch are in a clutch like formation and buried

underneath also increase survivalibility of the the species (Bernado et al, 2007).

This Photo by Unknown Author is licensed under CC BY-NC-ND. The Mouth of the
Kemp’s ridley sea turtle has a crushing surface and a beak like structure .
This Photo by Unknown Author is licensed
under CC BY-SA
The neck and limbs of the Kemp’s ridley is
covered with hard scales which provides
defence against predators. This is an
adaptation to its inability to take its neck
completely inside its carapace. Diagram
depicts the organism’s beak like mouth and
pores on the carapace

Anthropocene in relation to Kemp’s ridley sea turtles.

1. Issues:

The Kemp's ridley sea turtle population fluctuation has been evident throughout the course of

history, but in recent times, events which occurred at the start of the 19th century lead to a

population crash of Kemp's ridley sea turtles between the years 1947 to the early 1970's. This

could be the result of heavy industrialization, or multiple combinations of intense harvesting

of Kemp's ridley eggs by humans for consumption and economic profit (Reaves, 2012). The

mortality of juveniles caused due to extensive fishing of crabs and shrimps also contributed

to the drastic decline of Kemp's ridley population. In south american culture, sea turtle eggs

are considered a delicacy, people digging up and selling Kemp's ridley eggs rose in markets

between 1947 to the late 1960s (Reaves, 2012). The rest of the eggs which were dug up and

left by humans were consumed by predators as now the eggs were left without shelter. With
respect to adult Kemp's ridley sea turtles, prior to them being termed endangered, hunting

and fishing of Kemp's ridley was widespread and sold for meat and commercial ornamental

use (Reaves, 2012). Though as of recent protective measures have led to decrease in

poaching of Kemp's ridley, other human influences have made recovery of their population

even more difficult (Reaves, 2012). As Kemp's ridley primarily feeds on crabs and shrimps,

they often get caught in the fishing nets meant for crustaceans (Reaves, 2012). The highest

mortality rates are caused by fishing techniques as of today. Several steps are taken to

prevent this kind of mortality, with laws passed by Mexican and U.S fisheries to add Turtle

Excluder Devices to the fishing nets for allowing Kemp's ridley to escape (Reaves, 2012). In

the survey conducted by the fisheries department of Mexico and USA, the data stated that in

1947 the count of Kemp's ridley was approximately 89000 which dropped to a mere 7700 in

1985. Another report showed that nearly 12000 sea turtles drowned each year due to fishing

activities, mainly shrimp trawling (Reaves, 2012). Another issue faced by the Kemp's ridley

is debris collection in the ocean floor and surface. Debris is mistakenly consumed by fishes

and crustaceans and through bio-magnification, effluents enter the Kemp's ridley's system

causing digestive system disruption and nervous system failures (Reaves, 2012) . Effluents

are heavy mineral based or organic wastes. Kemp's ridley carcasses which wash up to the

shore have presence of ingested plastics and metal debris leading to digestive system failures

(Reaves, 2012). Much of this debris comes from offshore oil rigs and commercial and

recreational shipping vessels in the Gulf of Mexico. List of debris found in Debris-ingested

Kemp's ridley carcasses are - plastic bags, styrofoam, plastic pellets, balloons, rope, fishing

lines, glass, tar and alluminium foils (Reaves, 2012). Even though laws exists which prohibit

dumping of any debris in the ocean, the area of which the laws are enacted are so vast that it
is nearly impossible to keep check on any violations. This all comes down to human

lifestyles and our upbringing. If we are taught to respect nature since childhood, laws like

these and organisms dying from debris consumption would not be an issue to begin with.

One major issue which halted the recuperation of Kemp's ridley sea turtle population was oil

spills. The population of Kemp's ridley had a gradual increase at the start of the 21st century,

with population rising approximately over 15000 by 2009 (Reaves, 2012). The oil spills in

the Gulf of Mexico halted this progress. Along with affecting the habitat, the organisms on

which the Kemp's ridley depend on for food, the oil spills ingestion caused nervous system

failures in Kemp's ridley and Loggerhead sea turtles (Reaves, 2012).

This Photo by Unknown Author is


licensed under CC BY.
The Kemp’s ridley sea turtle
carcass found at the shore of
Mexico, covered in crude oil leaked
from oil rigs in the Gulf of Mexico.
Death by nervous system failure.
Management of Kemp's ridley sea turtles:

New research techniques should be developed and knowledge needs to be shared to increase

efficiency in management of this species. Not much data is available with respect to Kemp's

ridley sea turtle's population distribution and habitat usage behaviours (Reaves, 2012). The

life imprint and behaviours of Kemp's ridley sea turtles have limited data available on them

(Reaves, 2012). Most males have not been seen throughout the year, but show up during

mating season (Bernardo et al, 2007). The whereabouts of Kemp's ridleys who are yet to

sexually mature is difficult to locate and how they interact with other aquatic organisms is

still an undergoing study (Reaves, 2012). The study of migration patterns, drift lines,

foraging areas and consumption behaviour needs to be enhanced in order to developed

efficient management techniques and improve survivability of juveniles and hatch-lings

(Reaves, 2012). management of other organisms will also help in protecting the sea turtle

species. Managing crabs and shrimp fisheries on which Kemp's ridleys are primarily

dependent for food, will help eliminate the deaths by entangling and drowning within the net.

Turtle Excluder Devices are mandatory devices added to fishing nets which allow Sea turtles

to escape from the nets. Restricted laws on poaching have helped conservation of this

species by a great margin (Reaves, 2012).

I hereby conclude by saying that, several human influences have affected the populations of

Kemp's ridley sea turtles, but changes in lifestyles and changes in the ways we operate will

be the deciding point whether this endangered species survives the next fifty years or not.

With temperature a major limiting factor for Kemp's ridley sea turtles and the rapid change in

climate and increase in global warming needs us to come up with solutions and management

plans at an alarming rate.


This Photo by
Unknown Author is
licensed under CC
BY-NC
Turtle Excluder device
mechanism.
Difference between
traditional and TED
booted fishing nets.
References

1. Andrew D. Gentry. New material of the Late Cretaceous marine turtleCtenochelys acrisZangerl,

1953 and a phylogenetic reassessment of the ‘toxochelyid’-grade taxa. Journal of Systematic

Palaeontology, 2016; 1 DOI: 10.1080/14772019.2016.1217087

2. Bernardo, J. O. S. E. P. H., and PAMELA T. Plotkin. "An evolutionary perspective on the arribada

phenomenon and reproductive behavioral polymorphism of olive ridley sea turtles

(Lepidochelys olivacea)." Biology and conservation of ridley sea turtles (2007): 59-87.

3. Bowen, Brian W., Anne B. Meylan, and John C. Avise. "Evolutionary distinctiveness of the

endangered Kemp's ridley sea turtle." Nature 352.6337 (1991): 709.

4. Donald B. Brinkman, Patricia A. Holroyd, James D. Gardner. Morphology and Evolution of

Turtles. Springer Science & Business Media, 2012.

5. Dundee, Harold A. "The etymological riddle of the ridley sea turtle." Mar. Turtle Newsl 58

(1992): 10-12.

6. Lutz, Peter L., John A. Musick, and Jeanette Wyneken, eds. The biology of sea turtles. Vol. 2. CRC

press, 2002.

7. Reaves, TPWD Bill, and TPWD Mary E. Candee. "Kemp’s Ridley Sea Turtle." (2012).

8. Robertson, Douglas S., et al. "K‐Pg extinction: Reevaluation of the heat‐fire hypothesis." Journal

of Geophysical Research: Biogeosciences 118.1 (2013): 329-336.

9. Stacy, Michael. "Ancient Education." (2016).

10. Wilson, Paul A., and Richard D. Norris. "Warm tropical ocean surface and global anoxia during

the mid-Cretaceous period." Nature 412.6845 (2001): 425.

You might also like