Biotic impacts of energy development from shale: Research priorities and knowledge gaps

Abstract

Although shale drilling operations for oil and natural gas have increased greatly in the past decade, few studies directly quantify the impacts of shale development on plants and wildlife. We evaluate knowledge gaps related to shale development and prioritize research needs using a quantitative framework that includes spatial and temporal extent, mitigation difficulty, and current level of understanding. Identified threats to biota from shale development include: surface and groundwater contamination; diminished stream flow; stream siltation; habitat loss and fragmentation; localized air, noise, and light pollution; climate change; and cumulative impacts. We find the highest research priorities to be probabilistic threats (underground chemical migration; contaminant release during storage, during disposal, or from accidents; and cumulative impacts), the study of which will require major scientific coordination among researchers, industry, and government decision makers. Taken together, our research prioritization outlines a way forward to better understand how energy development affects the natural world.

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Rapid development of fossil-fuel resources has the
potential to transform landscapes and biological
communities before the resulting impacts are fully under-
stood. In the US, the extraction of gas and oil reserves
trapped in shale rock (known as “shale-gas” and “tight
oil”, respectively) through hydraulic fracturing (also
called “fracking” or “hydrofracking”) has grown exponen-
tially since 2007 (Figure 1; EIA 2011). Such technology
exploits previously inaccessible natural gas reserves
through the deep injection of high-pressure aqueous
chemicals into shale rock to create fractures, releasing
trapped gas (Figure 2; see “Additional references” section
in the web-only materials [WOM]). Although this tech-
nology is well studied (with >1000 peer-reviewed publi-
cations), surprisingly little research has focused on the
biotic impacts of shale development. While the biologi-
cal effects of other methods for extracting fossil fuels are
better understood, these studies generally lack clear
mechanistic links to fuel extraction and are limited to a
small number of species, countries, and ecoregions
(Northrup and Wittemyer 2012). Moreover, shale devel-
opment differs from other forms of fossil-fuel extraction
in multiple ways, including a broad and diffuse geo-
graphic footprint and an extremely high water demand.
Therefore, many of the biotic impacts of shale develop-
ment are unique and cannot be inferred from knowledge
of other forms of oil and natural gas extraction.
Understanding the impacts of shale development is
essential because many shale basins, particularly those in
the eastern US, occur in regions of exceptional biological
diversity (Figure 3); for instance, the most rapidly growing
source of natural gas in the US (ie the Marcellus Shale in
the Appalachian Basin) underlies one of the country’s
highest diversity areas for amphibians and freshwater fish
(Collen et al. 2013). In the US and Europe (Figure 4),
shale basins often overlap with areas already experiencing
severe threats to freshwater resources. In conjunction with
other anthropogenic activities, environmental change
associated with shale operations may cumulatively affect
living organisms in unknown, potentially calamitous, ways.
Here, we identify and prioritize research needs related
to shale development using a quantitative framework. We
consider the entire process of shale development, exam-
ining the threats to animals and plants from site develop-
ment and maintenance, water sourcing, well operation
and fracturing, and storage and disposal of injection fluids
(Figure 2). We classify impacts as probabilistic (ie
REVIEWS REVIEWS REVIEWS
Biotic impacts of energy development from
shale: research priorities and knowledge gaps
Sara Souther1*, Morgan W Tingley2, Viorel D Popescu3,4, David TS Hayman5,6,7, Maureen E Ryan3,8,
Tabitha A Graves9, Brett Hartl10, and Kimberly Terrell11
Although shale drilling operations for oil and natural gas have increased greatly in the past decade, few studies
directly quantify the impacts of shale development on plants and wildlife. We evaluate knowledge gaps related
to shale development and prioritize research needs using a quantitative framework that includes spatial and tem-
poral extent, mitigation difficulty, and current level of understanding. Identified threats to biota from shale
development include: surface and groundwater contamination; diminished stream flow; stream siltation; habitat
loss and fragmentation; localized air, noise, and light pollution; climate change; and cumulative impacts. We
find the highest research priorities to be probabilistic threats (underground chemical migration; contaminant
release during storage, during disposal, or from accidents; and cumulative impacts), the study of which will
require major scientific coordination among researchers, industry, and government decision makers. Taken
together, our research prioritization outlines a way forward to better understand how energy development affects
the natural world.
Front Ecol Environ 2014; 12(6): 330–338, doi:10.1890/130324
In a nutshell:
•Exploitation of oil and gas reserves trapped in shale rock,
including the extraction process known as “fracking”, poses
substantial and unexplored risks to living creatures
•Understanding the biotic impacts of operations that fracture
shale to access reserves is hindered by the unavailability of
high-quality data about fracturing fluids, wastewater, and
spills or violations
•The risks of chemical contamination from spills, deep well
failures, storage leaks, and underground fluid migration are
top research priorities
•Cumulative effects of shale development may represent the
most severe threats to plants and animals, but are particularly
challenging to study
1Department of Botany, University of Wisconsin, Madison,
Madison, WI *(ssouther@wisc.edu); 2Woodrow Wilson School,
Princeton University, Princeton, NJ; 3Earth to Ocean Research
Group, Department of Biological Sciences, Simon Fraser
University, Burnaby, Canada (continued on p 338)

S Souther et al. Research priorities for shale development
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© The Ecological Society of America www.frontiersinecology.org
unplanned or accidental) or deterministic (ie planned or
unavoidable) following the structure developed by Rahm
and Riha (2012). Our focus is on biota because plants,
animals, and other living organisms have largely been
omitted from other reviews, which tend to emphasize abi-
otic effects (eg Entrekin et al. 2011; Howarth et al.
2011a), and because shale formations often lie beneath
global hotspots of species diversity. Our goal is to improve
research of the biotic impacts associated with shale devel-
opment by prioritizing research needs and highlighting
associated challenges.
nPrioritization scheme
We assessed potential effects of shale development on liv-
ing organisms based on four criteria: current understand-
ing, spatial extent, temporal extent, and mitigation diffi-
culty (Table 1). For each impact, we ranked current
understanding as low, medium, or high and assigned a cor-
responding value of 3, 2, or 1 (where 3 is low understand-
ing, suggesting high research needs) based on the number
of relevant studies (additional methods provided in
WebPanel 1). The three remaining risk-based criteria were
assigned values of 1, 2, or 3, corresponding to low, medium,
or high ratings (where 3 represents high risk to biota for a
criterion). For each impact, the research priority was calcu-
lated by averaging criteria values, where current under-
standing was weighted by a factor of 3 to reflect the impor-
tance of existing scientific information in determining
research needs. Average values corresponded to final rank-
ings as follows: low (1.0–1.5), medium-low (1.6–1.9),
medium (2), medium-high (2.1–2.5), and high (>2.5).
nProbabilistic impacts
Probabilistic impacts to biota from shale development do
not occur as an unavoidable outcome of development but
do occur with a certain frequency. Although some of
these impacts may be rare occurrences (ie the result of
“unexpected” events), because most relate to the release
of potentially toxic chemicals into the environment, the
possibility of biotic harm can be great.
Underground migration of contaminants
During well fracturing, chemicals suspended in an aque-
ous medium are injected under high pressure into shale to
release natural gas. Fracturing fluid generally includes a
mix of acids, biocides, friction-reducing agents, and other
chemicals to facilitate gas retrieval (Vidic et al. 2013).
Many of the chemicals (eg methanol, xylene, naphtha-
lene, hydrochloric acid, toluene, benzene, and formalde-
hyde) are regulated in the US by the Safe Drinking Water
Act, the Clean Water Act (40 CFR Section 401.15), or
the Clean Air Act (US EPA 2012) and have been linked
to negative health effects in humans (Colborn et al.
2011). Releases of fracking fluid into streams have
resulted in direct mortality and stress of fish and aquatic
invertebrates (Papoulias and Velasco 2013). A propor-
tion of this fluid – the amount varies substantially among
geologic formations, but can be as high as 90% – remains
underground after its application (Entrekin et al. 2011;
Vidic et al. 2013). The fate and potential biotic impacts of
unrecovered fracturing fluids are highly uncertain.
Due to the depth of most hydraulically fractured shale-gas
formations (900–2800 m; Vidic et al. 2013), the contamina-
tion of groundwater by subsurface migration of fracturing
fluid is considered unlikely (Engelder 2011; Vidic et al.
2013). Nevertheless, geologic pathways for chemical migra-
tion have been identified (Warner et al. 2012). Moreover,
drinking water contamination with fracturing chemicals
and/or methane (CH4) has been reported (DiGiulio et al.
2011; Osborn et al. 2011; Jackson et al. 2013), although
some of these studies have been criticized as providing
insufficient evidence to attribute water contamination to
shale development (eg Davies 2011). Future research must
determine whether hydraulic fracturing causes CH4conta-
mination and whether, in the absence of equipment failure
and accidents, chemicals do migrate from fractured shale
beds. Given the limited understanding (WebTable 1) of the
likelihood, frequency, and spatiotemporal extent of such
contamination events, and the few options for mitigation,
this is a high research priority (Table 1).
Contamination from equipment failure, illegal
activities, and accidents
In addition to chemical migration from fractured shale,
freshwater contamination may result from well blowouts,
casing failures, illegal discharge, and spills during fluid
transport and storage (Figure 2). Many such contamina-
tion events involve the release of recovered fluid (called
“produced water”), which consists of fracturing fluid and
salts, heavy metals, hydrocarbons, and radioactive material
accumulated from natural underground sources (Howarth
et al. 2011a). The high saline content of recovered fluid
Figure 1. Proliferation of natural gas wells in the Jonah Field,
Wyoming, US. Inset: historical and predicted natural gas
production in the US. Data from EIA (2011).
EcoFlight

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alone poses risks to biota, given that increases in salinity
of as little as 1 g L–1 can harm or kill aquatic plants and
invertebrates (Hart et al. 1991).
Currently, the frequency and extent of freshwater contam-
ination due to spills, accidents, and violations is poorly quan-
tified. Of the 24 US states with active shale gas reservoirs,
only Pennsylvania, Colorado, New Mexico, Wyoming, and
Texas maintain public records of spills or violations for oil
and gas drilling operations. We examined the frequency and
nature of violations in the Pennsylvania Department of
Environmental Protection’s (PADEP’s) oil and gas manage-
ment compliance-reporting database (data analyzed in
WebTable 2). A total of 523 violations at 279 permitted wells
were detected in 2013, representing ~2.5% of inspections
(12 452 total) and 5% of wells (5580 total). The three most
common violations included: failure to properly store, trans-
port, process, or dispose of residual waste (n= 85); failure to
adopt required or prescribed pollution prevention measures
(n= 48); and failure to plug a well upon abandonment (n=
43). Spills were detected at 37% of wells found in violation
and were generally small (median = 265 L; range = 4–43 000
L), although there were nine spills of over 3500 L. Spills typ-
ically occurred on the well pad, with nearly
20% of reports documenting contamina-
tion of land or surface water. Location (on-
pad versus off-pad) was specified in fewer
than half of the reports (42%), and spatial
extent of contamination was rarely (5%)
described. The time between the spill and
reporting was noted in <10% of cases
(median = 5.75 hours; range = 1 hour to 6
weeks). In addition to the lack of data
describing the nature and extent of spills,
spill frequency was probably underesti-
mated. Many reports were ambiguous, and
companies routinely violated Pennsylva-
nia’s reporting requirement (only 59% of
documented spills were reported by the
drilling company). Collectively, poor data
quality and lack of consistent reporting
represent a major obstacle to understand-
ing the impacts of chemical contamina-
tion from shale development. Ecological
impacts of spills and accidents are also a
high research priority, given the limited
knowledge, the potential for lasting and
widespread adverse environmental con-
sequences, and the difficulty in mitigating
such contamination events.
Release of contaminants during
waste storage and disposal
As in the case of contamination from
spills and accidents, lack of data on
wastewater disposal impedes environ-
mental assessment. Waste volume, com-
position, and fate vary among drilling companies, states,
and geologic formations (Entrekin et al. 2011; Rozell and
Reaven 2011; Rahm and Riha 2012; Rahm et al. 2013).
Industry-reported data from PADEP revealed a 570%
increase in wastewater production since 2004 from devel-
opment of the Marcellus Shale (Maloney and Yoxtheimer
2012; Lutz et al. 2013). Drill cuttings were principally dis-
posed of in landfills, and wastewater (ie recycled fluid) was
most frequently treated at industrial facilities or injected
into deep wells (a large proportion of wastewater was re-
used prior to disposal; Maloney and Yoxtheimer 2012).
Risk of waste migration from deep injection wells to fresh-
water aquifers is poorly understood and, notably, deep well
injection has been linked to increased seismic activity
(Frohlich et al. 2011). Containment ponds frequently serve
as temporary wastewater storage at drilling sites, and these
vary substantially in structural integrity. Inadequately
designed ponds can overflow during heavy rain, may leak
as liners degrade, are accessible to wildlife, and are poten-
tial sources of air pollution as chemicals volatilize
(Entrekin et al. 2011). While the frequency of con-
tainment pond failure has not been quantified, our in-
Figure 2. Shale development includes multiple processes focused around natural gas
extraction via hydraulic fracturing. Impacts of shale development on biota can
include probabilistic (1, 6, 7, 8) and deterministic (2, 3, 4, 5, 9) effects of these
various processes. Contamination of aquatic and terrestrial systems may occur due to
spills, leaks, or accidents during hydraulic fracturing (6), waste storage (1, 8), and
transport (5). Permanent removal of water from the hydrologic cycle and subsequent
effects on water quality (9), habitat loss and fragmentation (4), and air (2) and
noise and light (3) pollution are unavoidable consequences of shale development,
although technological advances and appropriate planning can minimize biotic effects.
Shale development contributes to climate change in various ways, including CH4
release during well venting (2) as well as fossil-fuel use during site development, well
fracturing, and waste disposal (eg 5).
S Friedrich

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© The Ecological Society of America www.frontiersinecology.org
vestigation of Pennsylvania’s
2013 well inspection data
(described above) detected
numerous violations (eg 27
violations citing “Pit and
tanks not constructed with
sufficient capacity to contain
pollutional substances”), indi-
cating that some containment
facilities fail to prevent escape
of contaminants. Inappropri-
ate management of waste
products, including the direct
discharge of industrial waste
into streams, comprised 34%
of the total violations issued
by PADEP (WebTable 2).
There is virtually no empir-
ical information about the
biotic risks associated with
disposal of produced water
and drill cuttings (WebTable
1). Given this paucity of data,
the unquantified spatial and
temporal extent of contami-
nation, and few mitigation
options, the pathways and
consequences of environmen-
tal contamination from waste
storage and disposal represent
high research priorities (Table
1). A critical first step in this
research is improving basic
reporting to generate accurate
data describing waste compo-
sition and fate. For each
method of wastewater dis-
posal, future research should
determine the concentration
of toxins released into the
environment, exposure duration and potential pathways
(eg ingestion, inhalation, or contact), and the effects on
aquatic and terrestrial biota. A general evaluation of cur-
rent above- and belowground remediation strategies is
needed to address whether current technologies are capa-
ble of removing contaminants and what site characteristics
enhance or preclude effective remediation.
Disclosure of fracturing chemicals
Although not a biotic impact on its own, the lack of disclo-
sure regarding many fracturing chemicals can hamper the
ability of researchers to understand, predict, and mitigate
adverse environmental effects. Certain chemicals in frac-
turing fluids are classified as confidential business informa-
tion under Section 14(c) of the US Toxic Substances
Control Act (US EPA 2012). Many companies have vol-
untarily disclosed non-proprietary fluid components, and
ten states currently participate in the FracFocus
(www.fracfocus.org) national registry as a means of chemi-
cal disclosure. We investigated the proportion of propri-
etary components for 150 randomly selected wells repre-
senting three of the top producing states (ie Texas,
Pennsylvania, and North Dakota) in the registry (data
presented in WebTable 3). Overall, 67% of wells in our
sample were fractured with fluid containing at least one
undisclosed chemical, and 37% were fractured with five or
more undisclosed chemicals. Some wells (18%) were frac-
tured with a complex fluid containing 10 or more undis-
closed components. Importantly, many disclosed chemi-
cals lacked Chemical Abstracts Service (CAS) numbers
or concentration values. Most wells (82%) were fractured
with fluid containing either undisclosed components or
disclosed chemicals lacking this information. Chemical
Table 1. Research priorities based on the relative extent, difficulty mitigating, and
current understanding of potential impacts
Source of ecological Type of Spatial Temporal Mitigation Current Research
impact occurrence*extent** extent difficulty
understanding
†priority‡
Underground Unknown Unknown High Low High
migration of Probabilistic (3) (3) (3) (3) (3.0)
contaminants
Contamination of
surface water from Unknown Unknown High Low High
equipment failure, Probabilistic (3) (3) (3) (3) (3.0)
illegal activities,
and accidents
Release of
contaminants during Unknown Unknown High Low High
waste storage or Probabilistic (3) (3) (3) (3) (3.0)
disposal
Cumulative impacts Unknown Unknown Unknown Low High
Probabilistic (3) (3) (3) (3) (3.0)
Land application of Deterministic Low Medium Medium Low Medium-High
wastewater (1) (2) (2) (3) (2.3)
Climate-change Deterministic High High High High Medium
contribution (3) (3) (3) (1) (2)
Habitat Deterministic High High Medium High Medium-Low
loss/fragmentation (3) (3) (2) (1) (1.8)
Diminished stream Deterministic Medium Medium Low Medium Medium-Low
flow (2) (2) (1) (2) (1.8)
Air pollution Low Low Medium Medium Medium-Low
Deterministic (1) (1) (2) (2) (1.7)
Siltation Medium Medium Medium High Low
Deterministic (2) (2) (2) (1) (1.5)
Noise pollution Low Low Low High Low
Deterministic (1) (1) (1) (1) (1.0)
Light pollution Low Low Low High Low
Deterministic (1) (1) (1) (1) (1.0)
Notes: *Following Rahm and Riha (2012). **Values in parentheses correspond to numerical rankings, as explained in text. Box
color reflects the severity of each criterion, from minor (blue) to severe (orange). †Weighted by a factor of 3 to reflect impor-
tance of current knowledge in determining research priorities. ‡Final rankings in parentheses correspond to weighted average
of individual rankings.

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information was sometimes omitted for “non-hazardous”
components, but chemicals that are innocuous to humans
(eg some salts) can be lethal to freshwater organisms. No
chemical information was provided for produced water,
making it impossible to formulate these reclaimed fluids
for experimental research. A centralized source of chemi-
cal information would greatly facilitate research. The cur-
rent FracFocus registry has major limitations, including:
incomplete state participation; failure to consistently pro-
vide concentrations and CAS numbers for disclosed
chemicals; and non-disclosure of a substantial proportion
of chemicals. Because compounds in mixtures can have
synergistic or antagonistic effects (Altenburger et al.
2003), full chemical disclosure of fracturing fluid and
wastewater is essential for understanding the associated
risks to biota, including the effects of leaks, spills, and
direct terrestrial or aquatic application.
Cumulative impacts
The biological impacts of shale energy development are
numerous, and include water scarcity, habitat loss, and
various forms of pollution (see “Deterministic impacts”
section below). Many of these threats (Figure 2) cross ter-
restrial and aquatic boundaries, extend beyond the imme-
diate footprint of the operation, and may interact to
affect ecosystems in unexpected ways. Given that the
overall impact of shale development will likely outweigh
that of any individual stage of the process, risk assess-
ments should incorporate cumulative impacts on biota.
Importantly, this assessment framework should be
extended to consider the contributions of unrelated but
co-occurring stressors (eg resource extraction or residen-
tial development).
The few studies that consider cumulative impacts sug-
gest that shale-gas development will affect ecosystems on
a broad scale (Kiesecker et al. 2009; Jones and Pejchar
2013; Evans and Kiesecker 2014). For example, Evans and
Kiesecker (2014) found that energy development – pri-
marily from shale – in a large portion of the Marcellus
Shale could result in the construction of >500 000 ha of
impervious surface, leaving >400 000 ha of affected forest.
Given the overall absence of knowledge regarding cumu-
lative impacts, and the potential for synergistic, negative
interactions of shale-gas development impacts on ecosys-
tems, this area represents another high research priority
(Table 1). Using a cumulative-impacts framework,
researchers should specifically address how the density and
spatial configuration of shale wells interact with the tim-
ing and frequency of drilling operations (eg water with-
drawals or site clearing) to develop strategies for minimiz-
ing negative biological impacts. As cumulative impacts’
methodology and knowledge improve, research should
move toward detecting synergies between shale develop-
ment and other likely drivers of extinction, such as cli-
mate change, as site-specific or single variable risk assess-
ments likely underestimate threats to ecological health.
nDeterministic impacts
Most of the foreseeable ecological impacts of shale devel-
opment (eg pollution, habitat loss, siltation) are also asso-
ciated with other forms of anthropogenic disturbance.
While much knowledge can (and should) be drawn from
other disciplines, certain aspects of shale development
have unique temporal, geographic, spatial, and/or mecha-
nistic attributes. The challenge for the scientific commu-
nity is to determine what new information is needed to
understand and mitigate these impacts in the specific
context of shale development.
Siltation and diminished stream flow
Only 21% of river and stream length in the US is in “good
biological condition”, and major threats to freshwater
biota include siltation and water extraction (US EPA
2013b). Quantifying the effect of shale development on
siltation is difficult, but the factors that determine siltation
(eg well density and proximity to surface waters) are rela-
tively well studied. In the US, more than 6000 rivers are
impaired as a result of sediment pollution (US EPA 2014),
and the causes, consequences, and mitigation of siltation
have been studied for decades (Berkman and Rabeni 1987;
Donohue and Garcia Molinos 2009; Gellis and Mukundan
2013). The contribution of shale development to sediment
load will vary geographically, depending on local hydrol-
ogy, geology, and existing forms of land disturbance. In the
Marcellus region, habitats affected by shale development
are likely to include lower-order (eg headwater) streams
with relatively little sediment input from other sources
(Olmstead et al. 2013). Given the extensive amount of rel-
evant scientific literature about stream siltation
(WebTable 1), the moderate spatial and temporal extent of
this problem, and the existence of well-developed mitiga-
tion strategies as compared with other impacts, this threat
is a low research priority (Table 1).
While many forms of land use contribute to siltation,
shale development consumes an exceptionally large
quantity of fresh water. An average of nearly 20 million L
of water is required to fracture a shale well over its life-
time (Entrekin et al. 2011; Howarth et al. 2011a). Given
this massive water demand, well pads are typically con-
structed near freshwater sources. As of September 2010,
more than 750 shale wells had been drilled within 100 m
of rivers and streams in five eastern US states (Entrekin et
al. 2011), and nearly 4000 wells drilled within 300 m of
these freshwater habitats (Entrekin et al. 2011). The close
proximity of well sites to freshwater sources exacerbates
the risk of chemical contamination and sedimentation of
aquatic ecosystems (Gregory et al. 2011). Water extrac-
tion can substantially alter local hydrology by reducing
stream water levels and flow rates, which can result in
warmer water temperatures, increased concentrations of
pollutants, and less dissolved oxygen for aquatic life.
Certain aspects of freshwater removal for hydraulic frac-

S Souther et al. Research priorities for shale development
turing are unique (ie volume and geographic
pattern of water withdrawals). Although in-
stream flow is well studied in other contexts,
there is virtually no relevant empirical data
for shale development (WebTable 1). Given
the modest level of scientific understanding,
potential ease of mitigation (eg by restricting
water withdrawals), and relatively moderate
spatial and temporal extent, this threat repre-
sents a medium to low priority for research
(Table 1). The minimum stream flow rates
and water volumes necessary to sustain bio-
logical function will vary among habitats and
life stages, and should be studied at fine spa-
tial scales.
Habitat loss and fragmentation
Construction of wells and associated infra-
structure (eg access roads, pipelines) disrupts
habitat. On average, 1.5–3.1 ha of vegetation
are cleared during the development of a sin-
gle well pad (Entrekin et al. 2011). Although
this footprint is relatively small, the vast
number of shale wells equates to considerable
habitat loss. Furthermore, the amount of land
cleared for pipelines and other infrastructure
can far exceed that of the well pad
(Slonecker et al. 2012). In Pennsylvania’s
Bradford and Washington counties (together
representing ~280 000 ha of forest), shale-
drilling operations disturbed nearly 2500 ha
of land between 2004 and 2010, and dispro-
portionally affected the interior forests that
provide important habitat for rare species
(Slonecker et al. 2012); in the Susquehanna
River basin, more than one-quarter of shale
well pads were constructed in previously
intact forest habitat (Drohan et al. 2012). In
the western US, natural gas development has
decreased secure habitat for pronghorn
(Antilocapra americana; Bechmann et al.
2012) and mule deer (Odocoileus hemionus;
Sawyer et al. 2009), and disrupted breeding
sagebrush bird communities (Gilbert and
Chalfoun 2011) including greater sage-
grouse (Centrocercus urophasianus; Webb et al. 2012).
Well pads and infrastructure result in major habitat frag-
mentation. Shale development in known basins (Figures 3
and 4) threatens to disrupt ~500 natural corridors in west-
ern North America (Theobald et al. 2012). Such corridors
are crucial to maintaining healthy wildlife populations in a
changing climate (Lawler et al. 2013). While fragmentation
effects of shale development have been poorly studied
(Northrup and Wittemyer 2012), fragmentation from any
source can reduce dispersal, foraging, and mating success,
thereby increasing species’ risk of local extinction (Aguilar
335
© The Ecological Society of America www.frontiersinecology.org
et al. 2006; Fischer and Lindenmayer 2007). The resulting
edge habitat generally benefits common and generalist
species at the expense of rare and more vulnerable species
(Ries et al. 2004). Opening of formerly remote areas can
facilitate poaching of imperiled and sensitive species, serve
as a conduit for invasive and non-native species (including
pathogens), and provide a gateway to further and more per-
manent development (Fahrig 2003). Although habitat loss
and fragmentation occur on broad scales and are moder-
ately difficult to mitigate, these processes are relatively well
studied (WebTable 1) and represent a medium-low research
Figure 3. Freshwater biodiversity in relation to the extent of shale gas basins:
normalized species richness (a) globally and (b) within the US; US-only (c)
amphibian species richness, (d) crayfish species richness, and (e) fish species richness.
Biodiversity data (a–d) were derived from Collen et al. (2013); data in (e) were
derived from Hoekstra et al. (2010; downloaded from www.databasin.org and used
under a Creative Commons Attribution 3.0 License, http://creativecommons.
org/licenses/by/3.0). All freshwater biodiversity data are shown in relation to the
extent of shale gas basins assessed by the US Energy Information Administration
(www.eia.gov) and represent known extents as of May 2011; countries/regions
included in the global shale gas assessment are: Mexico, Canada, Colombia,
Venezuela, Argentina, Chile, Uruguay, Paraguay, Bolivia, Brazil, Algeria,
Tunisia, Libya, South Africa, France, Germany, Netherlands, Norway, Denmark,
Sweden, the UK, Poland, Ukraine, Lithuania, Romania, Bulgaria, Hungary,
China, India, Pakistan, Turkey, and Australia.
(a)
(b) (c)
(d) (e)

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priority (Table 1). Notably, however, new extraction tech-
niques have made it economical to develop historically
unprofitable gas reserves, threatening terrestrial biota in for-
merly intact areas (Northrup and Wittemyer 2012).
Moreover, the diffuse, branching pattern of habitat loss asso-
ciated with hydraulic fracturing distinguishes it from other
forms of land-use change (Northrup and Wittemyer 2012).
Light, noise, and air pollution
Shale operations create light, noise, and air pollution.
Anthropogenic light and noise can negatively affect fitness
across a broad group of species, including mammals, amphib-
ians, birds, insects, and aquatic invertebrates (see “Addi-
tional references” in the WOM). Noise pollution generated
by natural gas extraction causes some avian species to avoid
breeding sites (Blickley et al. 2012), resulting in reduced bird
abundance (Bayne et al. 2008). Shale operations emit nitro-
gen oxides (NOx), sulfur dioxide (SO2), carbon monoxide
(CO), volatile organic compounds (VOCs), and particulate
matter, each of which is harmful to biota (see “Additional
references” in the WOM). In addition to their
direct toxicity, NOxand VOCs contribute to
ozone (O3) formation. Natural gas operations
emit nearly 30 times the VOCs as compared
with coal operations, primarily during extrac-
tion and transport (US EPA 2013a). Ground-
level O3is a strong pulmonary and respiratory
irritant in mammals (Watkinson et al. 2001)
and negatively affects growth, reproduction,
and survival of plants (Karnofsky et al. [2005]
and references within). Dangerous concentra-
tions of surface O3have been detected near
large oil and gas operations (Martin et al. 2011),
including in winter (Carter and Seinfeld 2012).
As O3pollution is normally a warm-weather
problem, its potential impacts on animals and
plants as a year-round phenomenon are entirely
unknown.
Given the limited scale of noise and light
pollution, along with the ease of mitigation
and relatively well-developed state of knowl-
edge, these threats are low research priorities
(Table 1). Air pollution is a slightly higher
(medium to low) research priority because it is
more challenging to mitigate; thus, aspects
unique to shale development warrant further
study (eg wintertime O3).
Climate-change contribution
Shale development will affect biota indirectly,
but substantially, through climate change.
These impacts occur primarily through the
routine venting of CH4during well fracturing,
but also from the release of carbon dioxide
(CO2) and other greenhouse gases during site
development, fracturing, and waste disposal (Howarth et
al. 2011b, 2012; Petron et al. 2012). Climate change poses
one of the greatest global threats to biota (Thomas et al.
2004), has spatially and temporally expansive impacts, and
is extremely challenging to mitigate. However, because
greenhouse gases and the chemical basis for climate change
are well understood (WebTable 1), we rank this threat as a
medium research priority in the context of shale develop-
ment (Table 1).
Land application of wastewater
As of 2011, certain states – including West Virginia,
Arkansas, and Colorado – permitted wastewater disposal via
direct application to land or roadways, often as a de-icing
agent (Adams 2011). Direct land application guarantees
immediate and widespread contamination of ecosystems.
Land application of wastewater has caused rapid, complete
mortality of vegetation and 56% mortality of trees within 2
years (Adams 2011). Other research supports these findings
and indicates that even low concentration of wastewater
(a)
(b)
Figure 4. (a) Global and (b) US distribution of pre-existing threats to freshwater
biodiversity in relation to the extent of shale gas basins. The Incident Biodiversity
Threat index for freshwater biodiversity was derived by Vörösmarty et al. (2010;
downloaded from www.databasin.org and used under a Creative Commons
Attribution 3.0 License, http://creativecommons.org/licenses/by/3.0), and ranges
from 0 (lowest threat) to 1 (highest threat). Areas in white denote regions with an
average annual runoff <10 mm (see supplementary materials from Vörösmarty
et al. [2010] for full description).

S Souther et al. Research priorities for shale development
337
© The Ecological Society of America www.frontiersinecology.org
can alter species composition (DeWalle and Galeone 1990).
Because current understanding of this threat is limited, miti-
gation is difficult, and impacts can persist for several years
(Adams 2011), the impact of wastewater application is a
medium-high research priority (Table 1).
nConclusion
As the development of shale energy reserves continues to
expand, substantial knowledge gaps remain regarding
effects of these activities on plants and animals. Using
criteria related to the environmental risks and current
understanding of these impacts, we suggest that top
research priorities are related to probabilistic events that
lead to contamination of fresh water, such as equipment
failure, illegal activities, accidents, chemical migration,
and wastewater escape, as well as cumulative ecological
impacts of shale development (Table 1). Although other
threats are considered lower priorities, these rankings are
relative, general, and dependent on the scarce peer-
reviewed literature pertaining directly to shale develop-
ment (WebTable 1). Certain components of relatively
low-ranking threats (eg winter O3, air pollution) may
warrant greater prioritization, especially in particular
regions or ecosystems. Furthermore, these rankings are
based on the assumption that feasibility of mitigation
translates to effective mitigation. For example, water
scarcity has documented negative effects on aquatic
organisms, and can be avoided by managing water with-
drawals. Nevertheless, water management continues to
be a major conservation issue in water-limited ecosys-
tems. When the ecological consequences of shale devel-
opment are easily foreseeable (ie deterministic), research
focused on mitigation is generally a higher priority than
determining basic effects on biota. In other cases (eg land
application of wastewater), the need for research may be
circumvented by a change in state or federal regulation.
Given the rapid expansion of shale development, the
scientific community should prioritize research to exam-
ine threats with the greatest potential for biotic harm.
Here, we identify four high-priority research areas, but
acknowledge that these priorities are likely to change as
scientific understanding, government regulations, and
mitigation strategies develop. Rather than a rigid guide-
line, the approach presented here is a call to action for
scientists, industry leaders, and decision makers. We must
actively cooperate to understand the ecological risks asso-
ciated with shale energy development and work to mini-
mize its impacts on natural systems.
nAcknowledgements
We received support from the David H Smith Fellowship
program, administered by the Society for Conservation
Biology and funded by the Cedar Tree Foundation. BH was
supported by a Policy Fellowship from the Wilburforce
Foundation to the Society for Conservation Biology. An
early version of this manuscript was sent as a letter to the
US Geological Survey, the Environmental Protection
Agency, and the US Department of the Interior; we thank
these agencies for their review and assistance in improving
the manuscript. We also thank M Böhm and B Collen for
providing the freshwater species richness data, and S
Friedrich for graphic design of Figure 2.
nReferences
Adams MB. 2011. Land application of hydrofracturing fluids dam-
ages a deciduous forest stand in West Virginia. J Environ Qual
40: 1340–44.
Aguilar R, Ashworth L, Galetto L, and Aizen MA. 2006. Plant
reproductive susceptibility to habitat fragmentation: review
and synthesis through a meta-analysis. Ecol Lett 9: 968–80.
Altenburger R, Nendza M, and Schüürmann G. 2003. Mixture tox-
icity and its modeling by quantitative structure–activity rela-
tionships. Environ Toxicol Chem 22: 1900–15.
Bayne EM, Habib L, and Boutin S. 2008. Impacts of chronic
anthropogenic noise from energy-sector activity on abundance
of songbirds in the boreal forest. Conserv Biol 22: 1186–93.
Bechmann JP, Murray K, Seidler RG, and Berger J. 2012. Human-
mediated shifts in animal habitat use: sequential changes in
pronghorn use of a natural gas field in Greater Yellowstone. Biol
Conserv 147: 222–33.
Berkman H and Rabeni C. 1987. Effect of siltation on stream fish
communities. Environ Biol Fish 18: 285–94.
Blickley JL, Blackwood D, and Patricelli GL. 2012. Experimental
evidence for the effects of chronic anthropogenic noise on abun-
dance of greater sage grouse at leks. Conserv Biol 26: 461–71.
Carter WPL and Seinfeld JH. 2012. Winter ozone formation and
VOC incremental reactivities in the Upper Green River Basin
of Wyoming. Atmos Environ 50: 255–66.
Colborn T, Kwiatkowski KS, and Bachran M. 2011. Natural gas
operations from a public health perspective. Human Ecol Risk
Assess 17: 1039–56.
Collen B, Whitton F, Dyer EE, et al. 2013. Global patterns of fresh-
water species diversity, threat and endemism. Global Ecol
Biogeogr 23: 40–51.
Davies RJ. 2011. Methane contamination of drinking water caused
by hydraulic fracturing remains unproven. P Natl Acad Sci USA
108: E871.
DeWalle DR and Galeone DG. 1990. One-time dormant season appli-
cation of gas well brine on forest land. J Environ Qual 19: 288.
DiGiulio DC, Wilkin RT, Miller C, and Oberley G. 2011. DRAFT:
Investigation of ground water contamination near Pavillion,
Wyoming. Ada, OK: US Environmental Protection Agency,
Office of Research and Development, National Risk
Management Research Laboratory.
Donohue I and Garcia Molinos J. 2009. Impacts of increased sedi-
ment loads on the ecology of lakes. Biol Rev 84: 517–31.
Drohan PJ, Brittingham M, Bishop J, and Yoder K. 2012. Early trends
in landcover change and forest fragmentation due to shale-gas
development in Pennsylvania: a potential outcome for the
north-central Appalachians. Environ Manage 49: 1061–75.
EIA (Energy Information Administration). 2011. Annual energy
outlook. Washington, DC: US Department of Energy.
Engelder T. 2011. Should fracking stop? Counterpoint. No, it’s too
valuable. Nature 477: 271–75.
Entrekin S, Evans-White M, Johnson B, and Hagenbuch E. 2011.
Rapid expansion of natural gas development poses a threat to
surface waters. Front Ecol Environ 9: 503–11.
Evans JS and Kiesecker JM. 2014. Shale gas, wind and water:
assessing the potential cumulative impacts of energy develop-
ment on ecosystem services within the Marcellus Play. PLoS
ONE 9: e89210.
Fahrig L. 2003. Effects of habitat fragmentation on biodiversity.
Annu Rev Ecol Evol S 34: 487–515.

Research priorities for shale development S Souther et al.
338
www.frontiersinecology.org © The Ecological Society of America
Fischer J and Lindenmayer DB. 2007. Landscape modification and
habitat fragmentation: a synthesis. Global Ecol Biogeogr 16:
265–80.
Frohlich C, Hayward C, Stump B, and Potter E. 2011. The
Dallas–Fort Worth earthquake sequence: October 2008
through May 2009. B Seismol Soc Am 101: 327–40.
Gellis AC and Mukundan R. 2013. Watershed sediment source
identification: tools, approaches, and case studies. J Soils
Sediments 13: 1655–57.
Gilbert MM and Chalfoun AD. 2011. Energy development affects
populations of sagebrush songbirds in Wyoming. J Wildlife
Manage 75: 816–24.
Gregory KB, Vidic RD, and Dzombak DA. 2011. Water manage-
ment challenges associated with the production of shale gas by
hydraulic fracturing. Elements 7: 181–86.
Hart BT, Bailey P, Edwards R, et al. 1991. A review of the salt sen-
sitivity of the Australian freshwater biota. Hydrobiologia 210:
105–44.
Hoekstra JM, Molnar JL, Jennings M, et al. 2010. The atlas of global
conservation: changes, challenges, and opportunities to make a
difference. Berkeley, CA: University of California Press.
Howarth RW, Ingraffea A, and Engelder T. 2011a. Natural gas:
should fracking stop? Nature 477: 271–75.
Howarth RW, Santoro R, and Ingraffea A. 2011b. Methane and the
greenhouse-gas footprint of natural gas from shale formations.
Climatic Change 106: 679–90.
Howarth RW, Santoro R, and Ingraffea A. 2012. Venting and leak-
ing of methane from shale gas development: response to
Cathles et al. Climatic Change 113: 537–49.
Jackson RB, Vengosh A, Darrah TH, et al. 2013. Increased stray gas
abundance in a subset of drinking water wells near Marcellus
Shale gas extraction. P Natl Acad Sci USA 110: 11250–55.
Jones NF and Pejchar L. 2013. Comparing the ecological impacts
of wind and oil & gas development: a landscape scale assess-
ment. PLoS ONE 8: e81391.
Karnofsky DF, Pregitzer KS, Zak DR, et al. 2005. Scaling ozone
responses of forest trees to the ecosystem level in a changing
climate. Plant Cell Environ 28: 965–81.
Kiesecker JM, Copeland H, Pocewicz A, et al. 2009. A framework
for implementing biodiversity offsets: selecting sites and deter-
mining scale. BioScience 59: 77–84.
Lawler JJ, Ruesch AS, Olden JD, and McRae BH. 2013. Projected
climate-driven faunal movement routes. Ecol Lett 16: 1014–22.
Lutz BD, Lewis AN, and Doyle MW. 2013. Generation, transport,
and disposal of wastewater associated with Marcellus Shale gas
development. Water Resour Res 49: 647–56.
Maloney KO and Yoxtheimer DA. 2012. Production and disposal
of waste materials from gas and oil extraction from the Mar-
cellus Shale Play in Pennsylvania. Environ Pract 14: 278–87.
Martin R, Moore K, Mansfield M, et al. 2011. Final report: Uinta Basin
winter ozone and air quality study. Vernal, UT: Energy Dynamics
Laboratory, Utah State University Research Foundation.
Northrup JM and Wittemyer G. 2012. Characterising the impacts
of emerging energy development on wildlife, with an eye
towards mitigation. Ecol Lett 16: 112–25.
Olmstead SM, Muehlenbachs LA, Shih J-S, et al. 2013. Shale gas
development impacts on surface water quality in Pennsylvania.
P Natl Acad Sci USA 110: 4962–67.
Osborn SG, Vengosh A, Warner NR, and Jackson RB. 2011.
Methane contamination of drinking water accompanying gas-
well drilling and hydraulic fracturing. P Natl Acad Sci USA
108: 8172–76.
Papoulias DM and Velasco AL. 2013. Histopathological analysis of
fish from Acorn Fork Creek, Kentucky, exposed to hydraulic
fracturing fluid releases. Southeast Nat 12: 92–111.
Petron G, Frost G, Miller BR, et al. 2012. Hydrocarbon emissions
characterization in the Colorado Front Range: a pilot study. J
Geophys Res-Atmos 117: D04304.
Rahm BG and Riha SJ. 2012. Toward strategic management of
shale gas development: regional, collective impacts on water
resources. Environ Sci Policy 17: 12–23.
Rahm BG, Bates JT, Bertoia LR, et al. 2013. Wastewater manage-
ment and Marcellus Shale gas development: trends, drivers,
and planning implications. J Environ Manage 120: 105–13.
Ries L, Fletcher RJ, Battin J, and Sisk TD. 2004. Ecological
responses to habitat edges: mechanisms, models, and variability
explained. Annu Rev Ecol Evol S 35: 491–522.
Rozell DJ and Reaven SJ. 2011. Water pollution risk associated
with natural gas extraction from the Marcellus Shale. Risk Anal
32: 1382–93.
Sawyer H, Kauffman MJ, and Nielson RM. 2009. Influence of well
pad activity on winter habitat selection patterns of mule deer. J
Wildlife Manage 73: 1052–61.
Slonecker ET, Milheim LE, Roig-Silva CM, et al. 2012. Landscape
consequences of natural gas extraction in Bradford and
Washington Counties, Pennsylvania, 2004–2010. Reston, VA:
USGS. Open-File Report 2012–1154.
Theobald DM, Reed SE, Fields K, and Soulé M. 2012. Connecting
natural landscapes using a landscape permeability model to pri-
oritize conservation activities in the United States. Conserv
Lett 5: 123–33.
Thomas CD, Cameron A, Green RE, et al. 2004. Extinction risk
from climate change. Nature 427: 145–48.
US EPA (US Environmental Protection Agency). 2012. Study of
the potential impacts of hydraulic fracturing on drinking water
resources: progress report. Washington, DC: EPA.
US EPA (US Environmental Protection Agency). 2013a. 2008
national emissions inventory, version 3. Washington, DC: EPA.
US EPA (US Environmental Protection Agency). 2013b. National
rivers and streams assessment 2008–2009. Washington, DC:
EPA. EPA/841/D-13/001.
US EPA (US Environmental Protection Agency). 2014. National
summary of impaired waters and TMDL information. http://
iaspub.epa.gov/waters10/attains_nation_cy.control?p_report_
type=T#causes_303d. Viewed 15 Mar 2014.
Vidic RD, Brantley SL, Vandenbossche JM, et al. 2013. Impact of
shale gas development on regional water quality. Science 340;
doi:10.1126/science.1235009.
Vörösmarty CJ, McIntyre PB, Gessner MO, et al. 2010. Global
threats to human water security and river biodiversity. Nature
467: 555–61.
Warner NR, Jackson RB, Darrah TH, et al. 2012. Geochemical evi-
dence for possible natural migration of Marcellus Formation
brine to shallow aquifers in Pennsylvania. P Natl Acad Sci USA
109: 11961–66.
Watkinson WP, Campen MJ, Nolan JP, and Costa DL. 2001.
Cardiovascular and systemic responses to inhaled pollutants in
rodents: effects of ozone and particulate matter. Environ Health
Persp 109(S4): 539–46.
Webb SL, Olson CV, Dzialak MR, et al. 2012. Landscape features
and weather influence nest survival of a ground-nesting bird of
conservation concern, the greater sage-grouse, in human-
altered environments. Ecol Processes 1: 4.
4Centre for Environmental Research, University of Bucharest,
Bucharest, Romania; 5Department of Biology, Colorado State
University, Fort Collins, CO; 6Department of Biology, University
of Florida, Gainesville, FL; 7mEpiLab, Massey University,
Palmerston North, New Zealand; 8School of Environmental and
Forest Sciences, University of Washington, Seattle, WA;
9Department of Fish, Wildlife, and Conservation Biology, Colorado
State University, Fort Collins, CO; 10Society for Conservation
Biology, Washington, DC; 11Center for Species Survival,
Smithsonian Conservation Biology Institute, Front Royal, VA