BioRisk | 7 Fis | 8 (2022) Apeer-reviewed open-access journal

doi: 10.3897/biorisk.17.77438 RESEARCH ARTICLE & B lO RP IS k

https://biorisk.pensoft.net

Ecocide — global consequences
(pesticides, radionuclides, petroleum products)

Roumiana Metcheva!, Peter Ostoich', Michaela Beltcheva!

| Lnstitute of biodiversity and Ecosystem Research, Bulgarian Academy of Sciences, 1 Tsar Osvoboditel Blud.,
Sofia 1000, Bulgaria

Corresponding author: Roumiana Metcheva (rummech@yahoo.com)

Academic editor: S. Chankova | Received 1 November 2021 | Accepted 20 December 2021 | Published 21 April 2022

Citation: Metcheva R, Ostoich P, Beltcheva M (2022) Ecocide — global consequences (pesticides, radionuclides,
petroleum products). In: Chankova S, Peneva V, Metcheva R, Beltcheva M, Vassilev K, Radeva G, Danova K (Eds)
Current trends of ecology. BioRisk 17: 7-18. https://doi.org/10.3897/biorisk.17.77438

Abstract

The problem of environmental pollution is becoming increasingly important on a global scale. Man has
oversaturated the environment of his habitat with harmful and most often toxic waste. It is difficult to
describe all the toxic substances, as a separate book can be written for each group. The term “ecocide” has
been introduced, which reflects large-scale destruction of the natural environment. We will focus only

on three classes of pollutants that are of particular concern, creating environmental conflicts. These are:

¢ Pesticides are extremely toxic and create large amounts of non-degradable waste. It accumulates in
tissues and organs of target organisms, becoming toxic and causing serious pathological changes in the
body, mainly at the cellular and subcellular levels, causing various diseases and as a result, serious changes
in the structure and functions of the populations and the whole ecosystem are increasingly observed.

¢ Waste from the nuclear industry and radioactive fallout from nuclear explosions. It is especially
dangerous that radioactive elements can be concentrated in certain organs.

¢ Petroleum products - often large quantities end up in the seas and oceans, along with industrial
waste of various kinds, impossible to compensate for by nature and they pose a serious threat to ecosys-

tems, many of which have already been destroyed.

At the submolecular level, chemical and physical effects can lead to genetic rearrangements (muta-
tions); destructive ionization in the tissues of every living being, sometimes with completely unexpected
consequences for humans.

Keywords

Pesticides, petroleum products, radionuclides

Copyright Roumiana Metcheva et al. This is an open access article distributed under the terms of the Creative Commons Attribution License
(CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

8 Roumiana Metcheva et al. / BioRisk 17: 7-18 (2022)

Introduction

The word “ecocide” combines ‘eco’, which comes from ancient Greek word ‘owxoc’,
meaning house which nowadays means ‘habitat’ or ‘environment’ and -cide’ comes
from the Latin verb ‘caedere’, meaning ‘to cut down’ or ‘to kill’. Ecocide literally means
“to kill the environment’, or destruction of large areas of the natural environment as a
consequence of human activity.

The problem of environmental pollution is becoming increasingly important on a
global scale. Man has oversaturated the environment of his habitat with harmful and
often toxic waste. It is difficult to describe all the toxic substances, so the focus will
be stressed only on three classes of pollutants that are of particular concern, creating
environmental conflicts. These are:

1. Pesticides. Their use is sometimes unavoidable, yet they pose serious hazards to eco-
systems due to runoff in freshwater ecosystems and biomagnification along food chains.

2. Radionuclides. Localized anthropogenic contamination can be dangerous to
ecosystems due to a tendency of fission products such as '9'I, '°’Cs, and ?°Sr to bioac-
cumulate in the terrestrial and aquatic biota.

3. Petroleum and petroleum waste products. Large quantities of petroleum and its
derivatives have ended up contaminating ocean ecosystems and shorelines, producing
damage that is hard to overcome.

Ecocide can be irreversible when an ecosystem is damaged beyond its capacity for
self-repair. It is generally associated with damage caused by an organism, which might
cause ecocide directly by destroying enough species in an ecosystem to disrupt its struc-
ture and function. Ecocide can also result from pollution such as high concentrations
of pesticides which decimate the local biodiversity.

Pesticides

Pests are the most serious problem in agricultural production. Since the discovery of
DDT, farmers use pesticides as the most effective means against destruction of crop pro-
duction. Pesticides significantly damage the environment as well as humans, they damage
water and soil quality, which has a dangerous effect on animals, birds, plants and humans.

The degree of pesticide toxicity strongly depends on its environmental behaviour.
They enter in the ecosystems by two different pathways depending on their solubility.
Water-soluble pesticides enter groundwater, streams, rivers and lakes and in this way
harm non-target species. Fat-soluble pesticides enter organisms along food chains and
have a strong tendency towards biomagnification. They are absorbed in the fatty tissues
and result in persistence of pesticides in food chains for very long periods. These per-
sistent pollutants are transferred up the food chain faster than they are broken down or
are excreted. Therefore, the higher trophic levels of the food chains will contain higher

Ecocide - global consequences 2)

pesticide concentration. This disrupts the normal functioning of the whole ecosystem
as the species in higher trophic levels will die due to greater toxicity.

The threats associated with the use of these toxins cannot be ignored. It is of para-
mount importance to study the pesticide impact on populations of aquatic and terres-
trial ecosystems. Accumulation of pesticides along food chains is of greatest concern as
it directly affects terrestrial predators and raptors. Indirectly, pesticides can also reduce
the quantity of plants and primary consumers, on which higher orders feed. Spraying
with insecticides, herbicides and fungicides has also been associated with reduction in
the population of rare species of animals and birds.

Pesticides enter the water via rain, by runoff, leaching through the soil or they
may be applied directly to water surfaces, for instance, for the purpose of control-
ling mosquitoes. Water contaminated with pesticides is a serious threat to aquatic life
forms. It can affect aquatic plants, decrease dissolved oxygen in the water and can cause
physiological and behavioural changes in fish populations. These pesticides are not
only toxic themselves but also interact with stressors which include harmful blooms
of algae. Aquatic animals are exposed to pesticides in three ways: direct absorption via
skin; uptake via gills during breathing and via drinking contaminated water.

Pesticides in terrestrial ecosystems are able to cause sublethal and lethal effects on
plants. As early as 1977 Kelley and South (1977) note that herbicides cause considerable
damage to fungal species in soil by inhibiting the growth of symbiotic mycorrhizal fungi
that help plant nutrient uptake. Glyphosate, a broad-spectrum herbicide, reduces the
growth and activity of nitrogen-fixing bacteria in soil (Kanissery et al. 2019). Even low
doses of herbicides have a great impact on the productivity and diversity of the natural
plant communities and wildlife. Beneficial insects like bees and beetles can experience
significant population decline due to the use of broad-spectrum insecticides (Pisa et al.
2015). Synergistic effects of fungicides and neonicotinoid insecticides are very harmful
to bees. Even a low dose of them reflects negatively on their feeding behaviour. Since
2006, each year, honeybee populations have dropped by 29-36% (Pisa et al. 2015).

Some reports have confirmed that only about 10% of pesticides reach the target groups
of organisms in crops. (Pisa et al. 2015; WHO 2017) The majority of pesticides react with
non-target organisms (WHO 2017). If the toxicity expression of a pesticide is measurable,
the non-target organisms can be used as bioindicators. There are various options on the
choice of species for pesticide monitoring. They depend mostly on the feeding habitat of
the species. The non-targeted part of an applied pesticide moves through the ecosystem
and a significant portion of it accumulates in the lower trophic levels. By the mechanisms
of bioaccumulation, it reaches higher trophic level organisms and affects normal physiolog-
ical processes of the organisms, thereby putting the whole ecosystem at risk (EEA 2013).

Gutierrez et al. (2012) reported the response of the copepods and the cladocer-
ans as early bioindicators of endosulfan toxicity. Ecotoxicological risk to the copepods
Acartia margalefi, A. latisetosa and the mysid Siriella clausi can be used as early indica-
tors to assess the risk to marine ecosystems.

Due to specific morphological features, bees can carry pesticides which may be
brought to the hive. Thus beehives may also be polluted. The spraying of beehives

10 Roumiana Metcheva et al. / BioRisk 17: 7-18 (2022)

during honey collection may be the reason for pesticide adulteration of honey and bees-
wax (Kujawski and Namiesnik 2011). This indicates the use of honey bees as a potential
bioindicator to determine the amount of pesticide levels in pollinator communities.

Earthworms are common organisms in the soil ecosystem and play an important
role in soil health (Spurgeon et al. 2003). ‘They play a significant role as bioindicators of
soil contamination and as models for soil toxicity. Their reduction may alter the nutrient
cycling and nutrient availability to plants (Rizhiya et al. 2007). Pesticides produce neuro-
toxic effects in earthworms and after exposure they are strongly physiologically damaged,
with DNA damage, changes on feeding activity and loss of vitality (Zhang et al. 2020).

Bird feathers are one of the best indicators for the presence of pesticides in the body.
Several studies showed a significant correlation between the contamination level in sea-
birds’ food and their feathers. Feather collection is easy and minimally invasive and is
very important from the viewpoint of conservation biology. Moreover, feathers indicate
toxicant exposure during an annual cycle. There is a wide concentration range of pesti-
cides that can be traced using feathers from birds in Patagonia (6.49 + 5.95 ug/g) (Mar-
tinez-Lépez et al. 2015) to relatively high concentration in birds from Spain (870.48 +
614.48 ng/g) (Espin et al. 2012). Feathers can be used as bioindicators throughout the
wide range of different geographic regions of the world. For biomonitoring of OCPs in
Antarctica, penguin feathers are a very good tool (Metcheva et al. 2017).

A lot of studies show that herbivorous mammals, and especially rodents, are one
of the best species that fulfil the requirements for a good bioindicator for pesticide
contamination due to their large population number, good representation of spatial
and ecological niches, sufficient knowledge about their physiology, great reproductive
potential, as well as their dietary composition (Tataruch and Kierdorf 2003).

Since use of pesticides is unavoidable, early monitoring is essential to prevent or
control the damage caused by pesticides to humans and ecosystems. It is a timely need
to integrate the studies of different disciplines including toxicology, environmental
chemistry, population biology, community ecology, conservation biology and land-
scape ecology to understand the direct and indirect effects of pesticides on the envi-
ronment. In the future, chemical pesticides can be used in combination with natural
treatments and remedies, resulting in more sustainable elimination of pests. This com-
bination not only promises environmental health, but also has diverse applications in
controlling urban pests and invasive species.

Nowadays, is very important to control the use of pesticides and to find ways to
apply appropriate substances; to encourage farmers to reduce pesticide overuse. It is
necessary to develop and apply various techniques for remediation of pesticides from
the environment. Adsorption and bioremediation have been found to be most suitable
as environmentally friendly, cost-effective and less toxic by-products. Environmental
protection organisations, farmers, health professionals, producers, and governments
have to commit to and adopt joint initiatives to reduce the negative effects of pesti-
cides. Immediate action is needed to effectively control pesticides and to adopt strict
laws and regulations in this area. Integrated pest management is very useful for the
management and further application of pesticides, as well as for their best control.

Ecocide - global consequences 11

Radioactive contamination

Radionuclides are nuclides that have excess nuclear energy, making them unstable.
This instability is due to excess energy in the atomic nucleus, leading to the release of
particles with different energies in a process called radioactive decay. Natural radio-
nuclides emit alpha («), beta (8°) and gamma (y). Of these types, «-particles have the
strongest biological effects, causing 20 times more biological damage than an equiva-
lent dose of 8 or y radiation (ICRP 2007). While « and & particles do not penetrate
deeply into matter, y-radiation, especially at the higher end of the energy spectrum, has
high penetration. Biologically, « and 8 emitters are only relevant if incorporated into
living organisms, while y-emitters are relevant both as internal and external radiation
sources. Some technogenic radionuclides emit other types of radiation. Medical PET
isotopes such as '8F, ''C, '°N, '°O, are positron (8*) emitters. Other radionuclides such
as *°°Cf are capable of emitting neutrons. Both positron and neutron emitters require
special equipment for handling and detection of radiation sources (Hall and Giaccia
2006). Some radionuclides emit multiple radiation types. The technogenic radionu-
clide '°’Cs emits 8 particles at two energies: 511 and 1173 kiloelectronvolts (keV), and
y-rays at 661.6 keV.

The biological effects of radionuclides are mainly due to the emitted ionizing radia-
tion (IR). Researchers have elucidated the biological effects of high and medium doses
of radiation. However, low-dose effects are still insufficiently understood (Hall and
Giaccia 2006; Kosti 2019). Currently, IR risk is extrapolated linearly to the low doses
by using the Linear Non-Threshold (LNT) mathematical model (Trott and Rosemann
2000; Hall and Giaccia 2006). Other hypotheses include radiation hormesis, which is
the idea that small doses of radiation are beneficial due to the induced protective stress
responses (Schirrmacher 2021), and low-dose hypersensitivity, which is the assumption
that low doses of radiation are more mutagenic (Joiner 2001). While radiation hormesis
has been well researched recently (Shankar et al. 2006; Schirrmacher 2021) it has still
not been taken into account in radiation protection calculations, where every minimal
dose of radiation is assumed to carry a small but non-negligible risk (ICRP 2007). On
the other hand, the low-dose hypersensitivity hypothesis is supported by recent studies,
raising questions about the validity of current assumptions in radioprotection (Heuskin
et al. 2013). Organisms have different radiosensitivities. The champion of radioresist-
ance is the bacterium Deinococcus radiodurans, which can withstand an acute dose of
5000 Gy with almost no loss of viability. Similarly, tardigrades can withstand 5000 Gy
with 50% loss in viability (LD,,=5000 Gy). For comparison, the LD,, for humans is
around 6 Gy, for mice around 6.4 Gy, and for goats only around 2.4 Gy (Bond 1963).

A significant concern in radionuclide-contaminated areas arises from the process
of bioaccumulation. Similarly to other elements from their respective groups, radio-
isotopes are incorporated preferentially into different target organs and tissues. Thus,
*°Sr, an analogue of calcium, has a strong affinity for bone and hematopoietic tissue.
Some of the properties of the three most significant anthropogenic radionuclides are

presented below (Table 1):

12 Roumiana Metcheva et al. / BioRisk 17: 7-18 (2022)

Table |. The most significant anthropogenic radionuclides and their biological effects (data adapted from
Besson et al. 2009 and Holm 2006).

Radionuclide Symbol Half-life (4) Emitted radiation Target tissue _ Biological effects
Cesium-137 OX 30.17 years B- (511, 1173 keV), y (661.6 keV) nerve, muscle different cancers
Strontium-90 20ST 28.8 years pure B- (546 keV) Bone bone cancer, leukemia
lodine-131 1 8.02 days —B- (333.8, 606.3 keV), y (364.5, 636.9 keV) thyroid gland thyroid cancer

As evident from the table, the most significant environmental contaminants of the
above are '°’Cs and *°Sr due to their long half-lives and persistence in nature. '°'I was
only a very significant risk in the first year following the Chernobyl accident, causing
~4000 excess thyroid cancers in the most significantly affected populations of the for-
mer USSR (Williams 2006).

Natural radioactivity, including external terrestrial y-radiation, internal «, 8 and
y-radiation from terrestrial radionuclides, cosmic radiation, and exposure to radon
(°Rn) and thoron (Rn) and their radioactive progeny molecules accounts for ~95%
of the annual radiation dose for the terrestrial biota (Hall and Giaccia 2006; ICRP
2007). Globally, there are areas with high natural radiation, mostly due to thorium
(Th) deposits. Two such areas are Guarapari, Brazil, and Kerala in southern India.
The area of Ramsar, Iran, has increased natural radioactivity due to radioactive hot
springs containing *’Rn and its progeny. Although annual doses in these areas reach an
average of 35-40 mSv/a, compared to 3.6 mSv/a average in Europe, epidemiological
studies report no excess cancer risk (Dobrzynski et al. 2015; Kosti 2019).

In contrast, environmental contamination by man-made radionuclides poses se-
rious risks. The Chernobyl accident is the most prominent example of technogenic
environmental damage, although it is not the only one; Chernobyl caused significant
chronic morbidity and mortality in people and enormous damage to the environment
and economies in Europe. This is mostly due to ''I, '°’Cs, and ”°Sr, and their ten-
dencies for bioaccumulation and biomagnification in terrestrial ecosystems (Chesser
et al. 2001, UNSCEAR 2020). Although the Chernobyl accident is the best-known
example, there are other significant events in the period 1945-2011. The Fukushima
accident in 2011 presents a new precedent — the reactors in the plant were nearing the
end of their design life (UNSCEAR 2020). Since this is true for many of the currently
operating reactors, crumbling nuclear infrastructure may present a significant radia-
tion hazard in the future.

Some of the risks to ecosystems posed by radionuclide contamination are well
understood. They include, at high doses >1 Gy acute dose, teratogenesis in developing
embryos, stunted plant growth, visible damage to the flora and fauna. These are known
as deterministic effects, because they occur definitely after exposure to strong doses of
ionizing radiation and are dose-dependent. More worrying are the so-called stochastic
effects, which occur with a small probability even at low radiation doses. These in-
clude radiation mutagenesis and, as a consequence of it, radiation carcinogenesis (Hall
and Giaccia 2006; ICRP 2007). Based on data from mouse experiments and results
from the monitoring of survivors of Hiroshima and Nagasaki, it is estimated that the

Ecocide - global consequences 13

doubling dose of radiation-induced mutagenesis is 1 Gy; an acute exposure to 1 Gy
of y-rays doubles the spontaneously occurring rate of mutation (Russell et al. 1958).
However, this perspective is being challenged. For example, Goncharova and Ri-
abokon (1998) observed transmission of chromosomal damage in the progeny of wild
rodents from the vicinity of Chernobyl, indicating genomic instability. Another, more
recent venue of research with significant progress, is the radiation-induced bystander
effect (RIBE) phenomenon, in which non-irradiated cells show similar cytotoxicity
and genetic damage to their irradiated neighbours (Osterreicher et al. 2003; Wang et
al. 2018). The results from bystander effect studies generally support the theory of low-
dose hypersensitivity and highlight possible molecular mechanisms for increased radia-
tion risks in the low-dose range (Osterreicher et al. 2003; Wang et al. 2018). Dubrova
et al. (1996) report a higher mini- and microsatellite mutation rate in the children of
Chernobyl liquidators. The same concern was raised in a more recent study (Bazyka et
al. 2020). Both of these findings support the theory that even low doses of radiation
can be harmful to the biota. Radiation risk is still to be taken very seriously, and every
effort should be made to keep radioactive contamination of ecosystems to a minimum.

Petroleum products

All types of oil differ by their chemical composition, weight, prior refinement, con-
centration of heavy metals, sulphur, and other impurities. Oil spills involve accidental
contamination by oil ranging from various grades of crude oil to different refined
products, from heavy fuel oil to light, less persistent, but very toxic fuels. The chemical
composition of the spilled oil, and the associated weathering reactions, determine their
fate, behaviour, and impact in the marine environments. Oil spills are of great concern
due to the long period of oil and gas exploitation and the adverse impacts of the ma-
rine environment and these various undesirable repercussions have been documented.
(Murawski et al. 2021).

On February 15, 1996 the oil tanker “Sea Empress” lost 72,000 t of crude light
oil and 370 t of heavy fuel oil of her cargo in the North Sea. Over 100 km of coastline
were affected. Estimates suggest that overall, 200 km of coastline has been affected. A
further 25,000 tons of waste were created by the clean-up operation. The “Sea Em-
press” ranks as one of the world’s top 10 oil spills Johnson and Butt 2006).

The 2010 “Deepwater Horizon” oil spill is considered the largest marine environ-
mental disaster in North America. Over 200 million gallons of oil poured into the
Gulf and contaminated the coast. It is estimated that up to 170,000 people worked to
clean up the Gulf oil spill. This event is now considered to be the worst environmental
disaster in US history, with massive ecotoxic effects on sea life and human habitats. The
ecological effects were drastic and longstanding, affecting all biota of all trophic levels
ranging from microorganisms and algae to pelagic fish, marine invertebrates, mam-
mals, and seabird populations, marine mammals from whales to otters, and plankton
populations (Lee et al. 2015).

14 Roumiana Metcheva et al. / BioRisk 17: 7-18 (2022)

Crude oil releases the most harmful toxins into the water and air within a short
time. The rest of the toxins are broken down by microorganisms in the sea water, but be-
fore this, crabs, shellfish and fish concentrate toxins in their bodies. The toxins are then
bioaccumulated in higher trophic levels. It could take decades to understand how oil
affects the next generation of whales, coral, sea turtles, birds, fish, and other marine life.

The toxic effects of oil spills to wildlife can be categorized as lethal and sublethal.
Basically, assessments of environmental impacts of oil spills are based on evaluating
concentrations of pollutants required to kill 50% of individuals in test animals’ toxico-
logical experiments to estimate lethal concentrations or other effective concentrations
(Bejarano et al. 2014). In this way considerable research was conducted to assess tra-
ditional biomarkers of biological endpoints (Mitchelmore et al. 2020) and to develop
and apply suites of sublethal indicators of aquatic biota health in order to understand
the induction of health effects involving immune system function, genomic chang-
es, reproductive success, growth effects, and impairment of various organ systems in
affected species (Sherwood et al. 2017; Grosell and Pasparakis 2021; Rodgers et al.
2021). Most often, research on pollutant effects on gene expression is conducted with
model organisms. At the sub-molecular level, chemical and physical effects can lead to
genetic rearrangements (mutations); destructive ionization in the tissues of every living
being, sometimes with completely unexpected consequences for humans.

Ten years after it happened, the “Deepwater Horizon” oil spill continues to harm
wildlife. The spill affected 320 miles of shoreline and affected the rich and complex
ecosystem of the Gulf. The future duration and magnitude of that impact is uncertain,
principally because scientists do not know how the pollutants will affect the Gulf eco-
system in the long term. Observations of damaged corals indicate impact at a depth of
1,370 m, 11 km from the site of the blowout.

Deep-water colonial corals together with ophiuroid symbionts may provide a more
sensitive indicator of the impact from petroleum hydrocarbons. They are important
habitats for shrimp, crabs and other marine life. Coral colonies presented widespread
signs of stress, including varying degrees of tissue loss, sclerite enlargement, excess mu-
cus production, bleached commensal ophiuroids, and are covered by brown flocculent
material (floc).

Shellfish can digest oil, which could cause changes in reproduction, growth rates
or even death. Fish in oil spill areas show reduced reproduction even years after the
spill, because oil remaining in the environment is still toxic to fish larvae. Oil exposure
in fish can lead to cancer and eventually to death, but it can also result in reproductive
changes. Particularly the nesting habitats of sea turtles are affected. At least 402,000
were exposed to oil during the spill. Sea turtles are extremely sensitive to the effects
of contact with oil. Young and juvenile turtles have been found to starve to death
when their beak and oesophagus have become blocked with petroleum residue. Birds
were among the hardest-hit animals immediately after the spill. The oil coating their
feathers had reduced their ability to regulate their body temperatures due to feather
damage. Marine mammals face a more expansive threat than most other coastal biota
due to their large geographical range. Physical contact with oil has shown to have
substantial negative and lethal effects on many varieties of marine mammals, although

Ecocide - global consequences 15

the cumulative long-term effects of consumption of petroleum-laden food sources are
ongoing (Geraci 2012). Thousands of dolphins died in the months following the spill,
after they ingested toxins. They are important indicators of the overall health of the
ocean. Humans suffer from oil-related cancers. For many other species, the damage is
not clear. Many species have been difficult to study. That’s because scientists knew little
about the habits of many deepwater marine mammals before the spill, so have trouble
detecting changes from current data (Lee et al. 2015).

China, the United States, India and Russia are four of the world’s top polluters. At
least 10 countries have national ecocide laws, including Vietnam, which enacted the
law in 1990. Oil spills in remote high-energy locations will quickly disperse, and are
difficult to reach or remediate through dispersal methods. The removal methods are
expensive, labour-intensive, cause further environmental degradation, and are overall
ineffective (Lee et al. 2015).

Conclusions

The complete destruction of an ecosystem due to human activities may result from exploi-
tation of resources, nuclear warfare or the dumping of harmful chemicals. Ecocide includes
all major environmental disasters which would have severe consequences on the Earth’s
ecological system. Even years after the accidents it is still much too early to assess the full
impact. Decontamination will continue for a long period, probably more than 40 years.

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