Global Ecology and Conservation 13 (2018) e00365

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Global Ecology and Conservation

journal homepage: http://www.elsevier.com/locate/gecco

Review Paper

The flexible application of carrying capacity in ecology

Eric J. Chapman a, *, Carrie J. Byron b
a
Marine Science Center, University of New England, 11 Hills Beach Rd, Biddeford, ME 04005, USA
b
Marine Science Department, University of New England, 11 Hills Beach Rd, Biddeford, ME 04005, USA

a r t i c l e i n f o a b s t r a c t

Article history: Carrying capacity encompasses a broad collection of approaches used to better understand
Received 8 June 2017 biotic interactions in ecosystems and is often applied with no explicit regard to its his-
Received in revised form 1 December 2017 torical origin. In this paper, we reviewed the primary literature to examine how carrying
Accepted 21 December 2017
capacity is applied in ecology. We focused our review on ecosystem studiesdstudies that
frame their results at the ecosystem leveldpublished after the 1950s and highlight
Keywords:
emerging trends of this concept. We found that while carrying capacity offers some un-
Carrying capacity
derlying commonalities, a wide range of definitions and approaches hinders a unified
Conservation biology
Ecosystems
framework to better understand biotic ecosystem interactions. Not surprisingly, these
Ecosystem management studies most often use Kdthe number of individuals that the environment “can support”
Natural resources in a given areadto define carrying capacity, despite considerable ambiguity and uncer-
tainty in this approach. Furthermore, the studies that we reviewed spanned several levels
of ecological organization: molecules to communities and up to landscapes. To add further
complexity, it is not clear whether carrying capacity was intended as a dynamic concept
subject to temporal variability as it was often applied in the reviewed studies. We found
that carrying capacity is most often applied to studies in conservation biology, rangeland
and wildlife management, aquaculture, and fisheries biology. We explore ecosystem level
responses to implications of “carrying capacity” overshoot and discuss proposed mecha-
nisms that govern ecosystem carrying capacity. We discuss the usefulness of the concept
and end with suggestions to improve carrying capacity's general application in ecosystem
studies.
© 2018 The Authors. Published by Elsevier B.V. This is an open access article under the CC
BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/).

1. Introduction

Carrying capacity is a widely and commonly used concept among biologists to better understand biotic interactions with
and within a system, independent of the level of system organization (Monte-Luna et al., 2004). The evolution of the carrying
capacity concept is convoluted. Though carrying capacity is often attributed to the K variable in the logistic function from
Verhulst (Verhulst (1838); Equation (1))da model for population growthdVerhulst never employs the term "carrying ca-
pacity" (Sayre, 2008). The first use of Equation (1) in ecological applications has been attributed to both Lotka (1925) and Pearl
and Reed (1920). Equation (1) shows that the population size at a time t is dependent on: r the intrinsic rate of growth, N the
number of individuals, and K, historically referred to as the upper limit of growth.

* Corresponding author.
E-mail address: [email protected] (E.J. Chapman).

https://doi.org/10.1016/j.gecco.2017.e00365
2351-9894/© 2018 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/
licenses/by-nc-nd/4.0/).
2 E.J. Chapman, C.J. Byron / Global Ecology and Conservation 13 (2018) e00365

 
dN N
¼ rN 1  (1)
dT K

Nevertheless, carrying capacity has been extensively applied in a wide scale of studies, partially for its theoretical
simplicity and widespread familiarity within the biological research community. Because of its broad theoretical appeal and
potentially powerful applications in ecosystem management, it has been applied to a wide range of studies across scales. For
example, at the molecular or cellular level, carrying capacity has been applied to: 1) studies that model the number of mi-
crobes in the phyllosphere (Remus-Emsermann et al., 2012); 2) understand the influence of earthworms on the soil microbial
community (Groffman et al., 2015); and 3) link animal anatomy and physiology with hemoglobin oxygen carrying capacity
(Dabruzzi and Bennett, 2014; De Domenico et al., 2013; Tufts et al., 2013).
Despite its wide application today, most of the contemporary studies that use carrying capacity are unaware of its genesis
and historical application; in fact, the original application of carrying capacity is completely outside of the realm of biology. In
the comprehensive review of the subject, Sayre (2008) discusses carrying capacity as it was originally defined and applied;
carrying capacity was first applied in a mechanical engineering context to calculate the mass of a load that a steam ship could
carry (Fig. 1a). Now, engineers use the term “payload” to describe the “carrying capacity” or load that a physical object could
transport.
Carrying capacity was first applied to biological systems in the 1870s, however, it retained its literal application; in this use,
it referred to the mass of meat that pack animals could physically transport (Fig. 1a). Sayre (2008) attributes the evolution of
carrying capacity from a literal and quantitative concept to a figurative and qualitative concept from its application to live-
stock populations “being carried by the land where they lived” in the 1880s (Thomson, 1887). From this moment on, carrying
capacity referred to a quasi-quantitative amount of something that could be “carried by the environment.” The contemporary
usage of carrying capacity was further shaped in the 1950s from the logistic curve originally developed over 100 years prior
(Verhulst, 1838). In fact, it was not until the first edition of Fundamentals of Ecology when Odum (1953) assigned the term
“carrying capacity” to the asymptote of the logistic curve, though there was very little empirical evidence of such a thing
(Sayre, 2008). Before, according to Sayre (2008), the asymptote of the logistic curve was “simply an upper limit of
growth.” This new development undoubtedly influenced a generation of biologists, particularly at the population level of
ecologydthough there is considerable interest at several levels of ecological organizationdand continues to be widely
applied in the literature. This conceptual evolution of carrying capacity developed independently from the human carrying
capacity approach (see Vogt, 1948) that is commonly used in the sustainability and development literature, despite
sharing a common conceptual ancestor (Fig. 1a). In this study we focus on the former application of carrying capacitydthe
application more commonly associated with understanding biotic interactions in ecosystems that is independent of social
implicationsdin the context of intrinsic limits of populations in ecosystem studies.
Though there are benefits of using a widely applied and familiar conceptual approach to studying populations and eco-
systems, there are several limitations. For example, as discussed by Sayre (2008), carrying capacity (K) has never been
empirically shown in the field, “distinguishing between organisms and environment as factors determining population
growth was rendered intractable by the variability of environment itself.” Furthermore, there are theoretical issues raised by

Fig. 1. (a) Conceptual timeline of “carrying capacity” in the literature. “Carrying capacity” originated in the mechanical and engineering context. This review
focused on the application of carrying capacity approach as K, the intrinsic limit of a population. At some point in the late 19th century, carrying capacity evolved
from a quantitative literal concept to a qualitative figurative concept. Payload is defined as a load that a physical object could transport. (b) After carrying capacity
was assigned to the asymptote of the Verhulst (1838) equation in the 1950s, carrying capacity was widely applied in 5 different fields of ecosystems research.
Carrying capacity has been extensively applied in aquaculture, rangeland management, conservation biology, wildlife management, and fisheries biology.
 E.J. Chapman, C.J. Byron / Global Ecology and Conservation 13 (2018) e00365 3

the idea of a dynamic carrying capacity; as Sayre (2008) concludes: “if carrying capacity is conceived as static, it is theo-
retically elegant but empirically vacuous; but if it is conceived as variable, it is theoretically incoherent or at best question-
begging.” For decades, carrying capacity has been applied to ecology studiesdmostly at the population leveldwith very little
attention to the historical origins or the conceptual flaws in the approach.
Despite these weaknesses, carrying capacity continues to be an important construct for many ecological studies. In this
study we review how ecosystem studiesdin the years following the assertion by Odum (1953) that the asymptote of the
logistic curve is an environmental “carrying capacity”duse and define the carrying capacity concept, what governs ecosystem
“carrying capacity,” and what are the implications of overshooting the “carrying capacity” of an ecosystem. The aim of this
study was not to diminish or discredit ecosystem studies using carrying capacity. Instead, we sought to provide an overview of
ecosystem studies in the literature that use a carrying capacity framework to highlight specific commonalities within this
broad and often ambiguous approach. By doing so, we focus on fundamental ecological themes and principles that are often
missing from carrying capacity studies.
As much as carrying capacity provides an important theoretical lens to investigate biotic interactions with and within an
ecosystem, this concept raises many difficult to answer questions. For example, how is carrying capacity used in ecosystem
studies in the literature? More specifically: what information does the carrying capacity framework provide about an
ecosystem and biotic and abiotic interactions within an ecosystem? In this paper we ask the following questions: 1) is there a
unified approach to ecosystem studies using a carrying capacity framework; or more specifically; 2) what particular and
fundamental ecological concepts, principles, and metrics are tested, used, or applied in ecosystem studies that use carrying
capacity; and finally, 3) what are the mechanisms governing ecosystem carrying capacity? To answer these questions and to
highlight fundamental ecological principles often masked by the carrying capacity label, we conducted targeted keyword
searches in a peer-reviewed literature database and reviewed ecosystem studies that apply the carrying capacity framework.

2. Methods

To investigate how carrying capacity is applied to ecosystem studies in the literature, we conducted targeted keyword
searches in Scopus, a large database of peer-reviewed literature. We focused our initial search on papers published after 1953
through 2016. In 1953, Odum assigned the term “carrying capacity” to the asymptote (Odum, 1953)dup until then referred to
as “an upper limit of growth”dof the logistic equation developed by Verhulst (1838). By focusing on papers published post-
1953, we selected studies that conceptually linked carrying capacity and ecosystem level phenomena. We compiled a list of
1170 papers by searching for “carrying capacity” and “ecosystem.” We used the filter “ecosystem” to limit our review to papers
that discussed ecosystem level implications of carrying capacity, irrespective of the scale of the particular study. We refined
our search by focusing on articles published within the “environmental science” and “agricultural and biological sciences”
subject areas and we excluded studies in the “earth and planetary science” subject area. By doing so, we excluded a number of
studies (161) related to the global human population in an entirely different carrying capacity paradigm originally developed
by Vogt (Vogt (1948); (Fig. 1a)).
We examined the abstracts of the resulting 822 papers to limit our investigation to studies that explicitly tested carrying
capacity concepts using defined metrics. We looked for studies that explicitly: 1) defined carrying capacity; and 2) quantified
the carrying capacity in that particular study. We compiled and organized the studies that met these criteria (114 papers) into
three different tables by: 1) listing studies by how carrying capacity was defined (Table 1); 2) listing studies by factors or
mechanisms that govern carrying capacity (Table 2); and 3) listing studies that discuss the implications and the ecosystem
level response of exceeding carrying capacity (Table 3).

3. Results

Among the 114 papers that we reviewed, we found 5 major subject areas where carrying capacity is most often used and
applied: aquaculture, rangeland management, wildlife management, conservation biology, and fisheries biology (Fig. 1b). We
found that aquaculture studies accounted for 25% (29 papers) of the papers applying carrying capacity; combined, rangeland
management and wildlife management accounted for 42% (48 papers), fisheries biology/management accounted for 48% (55
papers), and studies in conservation biology accounted for 55% (63 papers). Summed, the subject areas exceeded the number
of papers we reviewed, as some papers spanned multiple subject areas. Of the 63 studies we reviewed in conservation
biology, 19 focused on at risk species including: the woodland warbler (Duarte et al., 2016), the numbat (Hayward et al., 2015),
and the African lion (Everatt et al., 2014; Kissui and Packer, 2004).

3.1. What exactly are we testing?

Across the disparate and wide-ranging ecosystem studies that use the carrying capacity framework, we found over 19
explicit permutations of carrying capacity with overlapping levels of similarity among the variations. Not surprisingly, most of
the applications quantified the number of individuals in an area, with or without explicitly acknowledging K as the historical
variable representing carrying capacity (Table 1; e.g. (Melero et al., 2014; Pool et al., 2014; Treydte et al., 2001)). Besides
studies that tested the number of individuals in a particular area with carrying capacity, we found studies that quantified: 1)
the oxygen carrying capacity of hemoglobin (Dabruzzi and Bennett, 2014; De Domenico et al., 2013; Tufts et al., 2013); 2) the
4 E.J. Chapman, C.J. Byron / Global Ecology and Conservation 13 (2018) e00365

Table 1
Explicit definitions of carrying capacity in ecosystem studies.

Definition of carrying capacity Study

Surface area Pagel et al. (2014)
Swan days (Swans*days) Wood et al. (2014)
Regression model relating lion density to Everatt et al. (2014)
biomass of preferred prey species
Number of individuals in an area Pool et al (2014), Aryal et al. (2014), Campos and Jack (2013), Gray et al. (2012), Nilsson et al. (2011),
Okayasu et al. (2011), Gliwicz et al. (2010), Cheyne (2006), Gaston et al. (2003), Zambrano et al. (2001),
Bjorndal et al. (2000), Comeau et al. (2015), Golluscio et al. (2015), Hayward et al. (2015), Huntsman and
Petty (2014), Moore (2013), Weckel and Rockwell (2013), Siamudaala et al. (2012), Peeters et al. (2010),
Perry and Bond (2009), Nedorezov et al. (2008), Perry and Schweigert (2008), Crawford et al. (2007),
Moran and Bjorndal (2005), Lo
pez-Sepulcre and Kokko (2005), Kissui and Packer (2004), Ruiz-Olmo et al.
(2001), Nagpal et al. (2000), Madenjian et al. (1998), Larsen and Hesthagen (1995)
Number of individuals in an area, K Melero et al. (2014), Fukasawa et al. (2013), Watari et al. (2013), Huang et al. (2012), Stewart et al. (2009),
Bradshaw et al. (2006), Hendriks et al. (2005), Pujoni et al. (2016), Duarte et al. (2016), MacCracken et al.
(2014), Braithwaite et al. (2012), Donovan et al. (2012), Zehnder and Hunter (2008), Hansen et al. (2007),
Flatt and Scheuring (2004), Byappanahalli et al. (2003), Nakamaru et al. (2002), Treydte et al. (2001),
Preston and Snell (2001), Kilmer and Probert (1977, 1979)
Rainfall and past temperature to infer large Rodríguez et al. (2014)
herbivore CC
Highest "sustainable" animal units per area/ Strassburg et al. (2014), Silva et al. (2011), Xu et al. (2011), Guyondet et al. (2010), Filgueira et al. (2014a,
production potential 2014b, 2014c), Ibarra et al. (2014), Byron et al. (2011), Ratan and Singh (2013), Filgueira et al. (2010),
Guyondet et al. (2014), Filgueira and Grant (2009), Grant et al. (1995), Das and Shivakoti (2006), Njoka and
Kinyua (2006), Jiang and Gibbs (2005), Ferreira et al. (1997), Smaal et al. (1997)
Spatial gradient of energy availability for Hurlbert and Stegen (2014)
individuals in an area
Biomass per area Feuereisel and Ernst (2009), García-Rubies et al. (2013), Heyman (1983), Kutlu et al. (2014), Lin et al.
(2013), Maury et al. (2007), The
bault et al. (2008), Wabnitz et al. (2010)
Syntaxonomic diversity Redzi

c (2007)
Size Mayer et al. (2006)
Mass of carbon per area Keith et al. (2010), Li et al. (2015)
Oxygen carrying capacity of hemoglobin Dabruzzi and Bennett (2014), De Domenico et al. (2013), Tufts et al. (2013)
Carrying capacity of greenhouse gas Worrall and Clay (2012)
emissions
Particulate organic carbon CC Sanz-L
azaro et al. (2011)
Soil water CC for vegetation Wang et al. (2008)
Foraging behavior Morris and Mukherjee (2007)
Organic CC for aluminum Cory et al. (2006)
Primary production for fishery Vasconcellos and Gasalla (2001)

Table 2
Factors governing carrying capacity in ecosystem studies. Though there is some thematic overlap in categories, we found over a dozen different mechanisms
governing carrying capacity in ecosystems.

Factors Governing Carrying Study

Capacity
Climate Heyman (1983), Guyondet et al. (2014), Scheidt and Hurlbert (2014)
Metabolizable energy Feuereisel and Ernst (2009), Filgueira et al. (2014a, 2014b, 2014c), Ismail and Jiwan (2015)
Energy Content/availability Jiang and Gibbs (2005), Perry and Schweigert (2008), The
bault et al. (2008), Guyondet et al. (2010, 2014), Peeters
et al. (2010), Wabnitz et al. (2010), Byron et al. (2011), Hurlbert and Stegen (2014), Wood et al. (2014)
Top down anthropogenic pressure García-Rubies et al. (2013), Everatt et al. (2014)
Habitat availability Gaston et al. (2003), Lo
pez-Sepulcre and Kokko (2005), Cheyne (2006), Perry and Bond (2009), Huang et al. (2012),
Donovan et al. (2012), Siamudaala et al. (2012), Braithwaite et al. (2012), Moore (2013), Campos and Jack (2013),
Watari et al. (2013), Fukasawa et al. (2013), Pool et al. (2014), Huntsman and Petty (2014), Strassburg et al. (2014),
Duarte et al. (2016)
Food availability Ferreira et al. (1997), Bjorndal et al. (2000), Nagpal et al. (2000), Byappanahalli et al. (2003), Moran and Bjorndal
(2005), Das and Shivakoti (2006), Grant et al. (1995), Morris and Mukherjee (2007), Crawford et al. (2007), Zehnder
and Hunter (2008), Filgueira and Grant (2009), Gliwicz et al. (2010), Xu et al. (2011), Jia et al. (2012), Ratan and Singh
(2013), Watari et al. (2013), Melero et al. (2014), Huntsman and Petty (2014), Filgueira et al. (2014a, 2014b, 2014c),
Hayward et al. (2015)
Prey availability Ruiz-Olmo et al. (2001), Zambrano et al. (2001), Aryal et al. (2014)
Primary productivity Smaal et al. (1997), Vasconcellos and Gasalla (2001), Bradshaw et al. (2006), Maury et al. (2007), Keith et al. (2010),
Worrall and Clay (2012), Rodríguez et al. (2014), Guyondet et al. (2014), Li et al. (2015), Golluscio et al. (2015)
Exposure to toxic substances Preston and Snell (2001), Nakamaru et al. (2002), Hendriks et al. (2005)
Omnivory/ Herbivory Golluscio et al. (2015), Pujoni et al. (2016)
Mortality Ibarra et al. (2014)
Hydrodynamics, water Larsen and Hesthagen (1995), Filgueira et al. (2014b)
temperature and flow
Nutrients Heyman (1983), Kutlu et al. (2014)
Disease Kissui and Packer (2004)
Frequency of sex Flatt and Scheuring (2004)
 E.J. Chapman, C.J. Byron / Global Ecology and Conservation 13 (2018) e00365 5

Table 3
The ecosystem responses of exceeding carrying capacity varied throughout the literature. Most of the implications found in the literature were related to a
decrease in ecosystem productivity.

Ecosystem Response Study

Decrease in biodiversity Gaston et al. (2003), The
bault et al. (2008), Stewart et al. (2009), Gliwicz et al. (2010), Sanz-

zaro et al. (2011), Huang et al. (2012), Watari et al. (2013), Pool et al. (2014), Socolar et al.
La
(2015)
Decrease in productivity Bjorndal et al. (2000), Moran and Bjorndal (2005), Grant et al. (1995), Perry and Schweigert
(2008), Wang et al. (2008), Filgueira and Grant (2009), Filgueira et al. (2010, 2014a, 2014b,
2014c), Byron et al. (2011), Ratan and Singh (2013), Weckel and Rockwell (2013), Rodríguez
et al. (2014), Wood et al. (2014), MacCracken et al. (2014), Ismail and Jiwan (2015), Comeau
et al. (2015), Golluscio et al. (2015)
Decrease in C sequestration (including increases in soil C Zehnder and Hunter (2008), Keith et al. (2010), Worrall and Clay (2012), Strassburg et al.
loss) (2014), Groffman et al. (2015)
Changes in biogeochemical cycling (e.g. C, N, P cycle Nagpal et al. (2000), Zehnder and Hunter (2008), Guyondet et al. (2010, 2014), Filgueira et al.
dynamics) (2010), Kutlu et al. (2014)
Increase in non-native invasions Watari et al. (2013), Fukasawa et al. (2013), Melero et al. (2014), Comeau et al. (2015)
Ecosystem state change, trophic cascade/ interactions, Kilmer and Probert (1979), Vasconcellos and Gasalla (2001), Zambrano et al. (2001), Jiang and
ecosystem collapse, ecosystem destability Gibbs (2005), Mayer et al. (2006), Filgueira et al. (2014a)

“sustainable” production carrying capacity of several commercially important animals, where “sustainable” is defined based
on context specific parameters, such as level of phytoplankton depletion (Filgueira et al., 2010, 2014a; Guyondet et al., 2014;
Strassburg et al., 2014; Xu et al., 2011); 3) the carrying capacity of game, given a particular biomass of plants in a given area
(Feuereisel and Ernst, 2009; Wabnitz et al., 2010), though when carrying capacity was first applied to biological systems, the
concept was applied to mostly mobile animals and not plants; and 4) the carrying capacity biomass for animals in a given area
(García-Rubies et al., 2013; Lin et al., 2013). We also found several categories of lesser-used carrying capacity studies based on:
1) surface area (Pagel et al., 2014); 2) syntaxonomic diversity (Red zi
c, 2007); 3) soil water carrying capacity to support plant
primary productivity (Wang et al., 2008); 4) the carrying capacity of carbon in a particular ecosystem (Keith et al., 2010; Li
et al., 2015); and 5) energy carrying capacity (Hurlbert and Stegen, 2014).

3.2. Molecules to landscapes

Carrying capacity is applied across all scales of ecological organization (Monte-Luna et al., 2004). Out of the 114 papers that
we analyzed, 2% used carrying capacity at the cellular/molecule level (3 papers), 59% at the population level (67 papers), 2% at
the community level (3 papers), 35% at the ecosystem level (40 papers), and less than 1% at the landscape level (1 paper). As
an exampledand perhaps most true to its historical applicationdas previously mentioned above, carrying capacity has been
applied at the molecular level to describe the oxygen carrying capacity of hemoglobin and how that relates to animal anatomy
and physiology (Dabruzzi and Bennett, 2014; Tufts et al., 2013).

4. Discussion

The high number of studies in rangeland and wildlife management suggests that the contemporary usage of the carrying
capacity concept is informed by its historical evolution. For example, as we discussed above, one of the first applications of
carrying capacity in the figurative sense was to discuss rangeland productivity and cattle grazing on grasslands (Thomson,
1887). In their review of range science, Sayre and Fernandez-Gimenez (2003) highlighted the evolution of carrying capac-
ity and its adoption in rangeland management ultimately from the engineering “payload” context. Our results suggest that the
historical use of carrying capacity has continued to inform its importance to the rangeland and wildlife management fields
today.
Concepts such as population size, “carrying capacity,” and population dynamics have long been central in the fields of
wildlife management and conservation biology (Shaffer, 1981). Because conservation biology is often concerned with single
species at risk for extinction and focus on the population level, it is intuitive that these studies use carrying capacity to
investigate species viability. Given that conservation biologists and wildlife managers are historically most often interested in
populations and dynamics of populations, including concepts such as birth rates, death rates, and Kdthe intrinsic limit of a
populationdthe application of carrying capacity in wildlife management and conservation biology is a natural extension and
application of the concept.
Though we found that the majority of the contemporary usage of carrying capacity was in subject areas that have a legacy
of application, ecosystem studies in aquaculture have recently adopted carrying capacity. For example, the earliest applica-
tions of an explicitly defined approach using carrying capacity in aquacultural ecosystems we found in this studydthere are
earlier examples of carrying capacity used in aquaculture studies (see Carver and Mallet, 1990; Incze et al., 1981)dwas in 1997
when four papers appeared in the same issue of Aquatic Ecology (Dame and Prins, 1997; Dowd, 1997; Ferreira et al., 1997;
Smaal et al., 1997). These studies focused on quantifying potential bivalve biomass for culture and discussed bivalve car-
rying capacity in terms of “water mass residence time, primary production time, and bivalve clearance time” (Dame and Prins,
6 E.J. Chapman, C.J. Byron / Global Ecology and Conservation 13 (2018) e00365

1997). In contrast to conservation biology and rangeland and wildlife management, the use of carrying capacity in ecosystem
studies within aquaculture is a more recent phenomenon. Though the carrying capacity concept has clear theoretical origins
and is attributed to the logistic function of Verhulst (1838) and the Odum (1953) assertion that the asymptote of the logistic
curve is a “carrying capacity,” the contemporary definition of carrying capacity is wide-ranging and its application extends
beyond the number of individuals in a given space.

4.1. Carrying capacity across scales of biological organization

Carrying capacity is most often used at the population level to describe an ecosystem's ability to “support” a specific and
often fixed number of species. At this level, we found a range of studies that: 1) modeled a range of moths that a plant could
support (Nedorezov et al., 2008); 2) quantified the carrying capacity of perennial grass (Fowler and Pease, 2010); 3) quantified
the impacts of climate change on the white throated dipper (Nilsson et al., 2011); and 4) modeled the impacts of fishing on
marine mammals in the management context (Moore, 2013).
Though energy flow is not often explicitly considered in population level studies, Akbaripasand et al. (2014) explicitly
investigated the metabolic demand required of a single species of fish. They quantified the energy budget of a species of fish in
a stream ecosystem. Given that population dynamics are often modeled with the equation attributed to Verhulst (1838), the
relatively high number of population level studies that use the carrying capacity concept was not surprising.
At higher levels of ecological organizationdcommunity, ecosystem, and landscapedthe carrying capacity concept is often
modified to explicitly incorporate principles of community competition, ecosystem energy flows or material cycling, and
landscape patches and pattern, depending on the scale of study. For example, in one of the few community level studies using
carrying capacity, Pagel et al. (2014) quantified waterfowl metacommunity recovery using a “nested subsets” theory following
ecosystem protection, a theory that measures ecosystem structure by analyzing either species-site interaction or species-
species interactions. In another study, Hurlbert and Stegen (2014) used community metrics, such as species richness and
phylogenetic structure to analyze the relationship between ecosystem energy availability and species richness. In the final
community level study we found in our search, Leary and Petchey (2009) tested the “insurance hypothesis”dthe idea that
increasing species richness has a stabilizing effect on communities and ecosystemsdin laboratory microcosms.
At the ecosystem level, we found studies that used carrying capacity to investigate fundamental principles in ecosystems
such as energy flow and material cycling. This includes studies that: 1) used a Dynamic Energy Budget (DEB) ecosystem model
to investigate the impacts of shellfish on the marine food web (Filgueira et al., 2014b; Guyondet et al., 2010; Peeters et al.,
2010); 2) quantified the magnitude of grazing at which the flux of greenhouse gas was equal to the sink of peat soils
(Worrall and Clay, 2012); and 3) used various permutations of quantifying the mass of carbon that a particular ecosystem can
sequester (Keith et al., 2010; Li et al., 2015) or in the case of fish farming, the load and impact of organic carbon deposition on
the benthos (Sanz-La
zaro et al., 2011). At the ecosystem level in the Patagonian steppe, rangeland carrying capacity has been
defined as a function of aboveground net primary production (ANPP), a “sustainable harvest” index, and as the fraction of
ANPP consumed (Golluscio et al., 2015). When carrying capacity is applied to ecosystem level studies, it is modified to test
principles of ecosystem ecology, such as the movement of energy and matter through the system.
We found only 1 study in our review that applied carrying capacity at the landscape level. Donovan et al. (2012) used a
concept borrowed from graph theory and habitat suitability maps to quantify the number of individuals in an area that any
given landscape may support. For example, Donovan et al. (2012) calculated the number of ovenbirds and bobcats that could
coexist in a given northeastern landscape area based on a maximum clique analysis, a computationally intensive analysis
based on habitat suitability maps for each species. Carrying capacity is rarely applied to landscape level studies, and we
speculate that this may be attributed to the difficulty of incorporating landscape principles in a carrying capacity context or
modifying carrying capacity concept for landscape analyses.
Despite the theoretical origin of carrying capacity and its use to model species interactions and population dynamics at the
population level, our results suggest that carrying capacity is widely used across all levels of ecological organization (see also
Monte-Luna et al., 2004). Our results also suggest that carrying capacity is modified to incorporate principles of each level of
ecological organization for which it is applied: 1) at the molecular level, atoms are the subjects “carrying”; 2) at the popu-
lation level, numbers of species and the interaction of species is of interest; 3) at the ecosystem level, the carrying capacity
incorporates energy and materials; and 4) at the landscape level, patches and patterns are incorporated.

4.2. Carrying capacity over time and space

While the logistic equation from Verhulst (Verhulst (1838); Equation (1)) may be used to model changes in population
sizes over time, it is unclear whether carrying capacity should be understood as a fixed entity as it was originally applied
(Fig. 1a), or as variable as it has been commonly applied since Odum (1953) named the asymptote of the logistic curve as
“carrying capacity” (Sayre, 2008). In our review, we found considerable differences among the reviewed studies with how
time and space are considered. For example, we found studies that implicitly and/or explicitly explored the variation of a
carrying capacity over time and space (Duarte et al., 2016; Groffman et al., 2015; Pujoni et al., 2016). We also found studies
that did not implicitly or explicitly consider variation of carrying capacity over time and space (Golluscio et al., 2015; Ismail
and Jiwan, 2015). In studies that considered carrying capacity dynamic with respect to time, scenarios or simulations were
most frequently used to quantify the variation in populations and in carrying capacity (Filgueira et al., 2014b; Ibarra et al.,
 E.J. Chapman, C.J. Byron / Global Ecology and Conservation 13 (2018) e00365 7

2014; Melero et al., 2014). For example, in their study to model production potential of shellfish through aquaculture, Ibarra
et al. (2014) implemented several one year simulations of mussel population dynamics by varying the initial mussel stocking
density. Ibarra et al. (2014) defined production carrying capacity as “the smallest initial mussel density that produced the
highest harvest yield.” At the end of their one-year simulations, they found highest production carrying capacities at in-
termediate stocking densities because food limitation led to a decrease in production carrying capacity at high initial stocking
densities. Given the goals of mussel producers, the emphasis on production carrying capacity is largely an economic rationale.
To account for temporal and spatial population variability in their study of production potential in oysters, Filgueira et al.
(2014b) used a spatially explicit ecosystem model to simulate the effects of bivalve grazing on phytoplankton. Stocking filter
feeders, such as bivalves, at high density negatively impacts the phytoplankton in the system and often limits shellfish
production (Grant et al., 1995; Ulanowicz and Tuttle, 1992). Filgueira et al. (2014b) used 5 scenarios to quantify the impacts of
increasing the standing stock biomass of oysters on phytoplankton and determined the carrying capacity of oysters based on a
depletion index of phytoplankton. Using the bay scale index of phytoplankton depletion, Filgueira et al. (2014b) demonstrated
how spatial variability within an ecosystem influences the production carrying capacity of shellfish. Given that the number of
individuals that an ecosystem can supportda concept in population biology with ties to carrying capacitydis strongly linked
with ecosystem productivity and that ecosystem productivity is spatially variable, it is not surprising that many of the studies
that we reviewed explicitly considered the spatial dependence of carrying capacity.

4.3. Mechanisms governing CC

Despite the ambiguity, wide-ranging, and multidisciplinary application of carrying capacity, our review of the literature
revealed several common mechanisms that govern carrying capacity, either explicitly or implicitly. That is, a large proportion
of the studies we reviewedd83 out of the 114 studiesddiscussed controls that governed carrying capacity in the context of
that specific study (Table 2). Fundamentally and perhaps unsurprisingly, we found that carrying capacity was controlled by
resource availability. However, several more specific mechanisms govern carrying capacity and highlight the extent that
carrying capacity is modified in a context-specific manner. For example, we found that food, space, and available energy were
the most common regulators of carrying capacity, accounting for nearly halfd41 out of 83dof the studies that identified a
carrying capacity control, although more than a dozen mechanisms have been proposed to govern carrying capacity in
ecosystems.
In general, studies that used carrying capacity in an animal production perspective (i.e. to maximize biomass for con-
sumption)dthe rangeland management and aquaculture fieldsdwere more likely to discuss food as a limitation of ecosystem
production and a control of ecosystem carrying capacity.
Another emergent and prevalent control over ecosystem carrying capacity was habitat or space availability. Space has been
reported to be a regulator of carrying capacity for moths (Nedorezov et al., 2008), fish populations in marine systems and
freshwater streams (Perry and Bond, 2009; Perry and Schweigert, 2008), and ungulate population size over geological scales
(Rodríguez et al., 2014). The importance of space or habitat for regulating carrying capacity was prevalent in the conservation
biology literature. For example, space availability is an important mechanism governing carrying capacity for: snow leopard
biomass in conservation areas (Aryal et al., 2014); the biomass of Ecuadorian Capuchin in fragmented forests (Campos and
Jack, 2013); and understanding reintroduced numbat population dynamics in Australia (Hayward et al., 2015). To combat
the risks of species extinctions, conservation biologists often propose conserving high-value habitat (Noss et al., 1997). For this
reason, it is not surprising that studies in conservation science often specify habitat or space as a factor governing carry
capacity. In other words, habitat and space are often used as currencies for endangered species conservation. To interpret this
more literally, space in conservation science is akin to biomass production in bivalves or money for a business. Although the
carrying capacity approach houses a spectrum of diverse studies and research fields, carrying capacity is fundamentally
governed by resource availability and specific governing factors depend on study and context.

4.4. Implications of CC overshoot

Among the ecosystem studies that we reviewed, many implications of “overshooting” the ecosystem carrying capacity
were discussed. While our analysis did not consider the effects of the duration of carrying capacity overshoot, we provide a
conceptual overview of the ecosystem level effects of carrying capacity overshoot (Fig. 2) and a list of studies that address
implications of exceeding ecosystem carrying capacity (Table 3). The most common ecosystem-level implications of over-
shooting carrying capacity in the studies that we reviewed were: 1) a decrease in species biodiversity and richness (Sanz-
L

bault et al., 2008); 2) a decrease in primary productivity (Byron et al., 2011;
azaro et al., 2011; Socolar et al., 2015; The
Perry and Schweigert, 2008; Ratan and Singh, 2013); 3) changes in biogeochemical cycling (Filgueira et al., 2010;
Groffman et al., 2015; Guyondet et al., 2010, 2010); and 4) an increase in the vulnerability to invasions (Comeau et al.,
2015; Fukasawa et al., 2013; Melero et al., 2014). In addition to these 4 commonly discussed implications of overshooting
carrying capacity, several studies discussed decreases in carbon sequestration (Groffman et al., 2015; Strassburg et al., 2014;
Zehnder and Hunter, 2008).
Several studies have suggested that overshooting carrying capacity may lead to larger magnitude ecosystem impacts. For
example, we found studies that discussed large scale ecosystem change, such as ecosystem state/regime change/thresholds in
8 E.J. Chapman, C.J. Byron / Global Ecology and Conservation 13 (2018) e00365

Magnitude of ecosystem level response

Vulnerability
to invasions
Richness
Productivity
Biodiversity
C sequestration

State B
Vulnerability
to invasions
Richness
Productivity
Biodiversity
C Sequestration Threshold
State A

Fig. 2. Implications of “overshooting” the carrying capacity in reviewed ecosystem studies. Most reviewed studies report a decrease in ecosystem productivity
and biodiversity as implications of overshooting carrying capacity. If the magnitude of overshoot is great enough, the ecosystem passes a threshold (dotted line)
and changes ecosystem state (different color of oval), where continued carrying capacity overshoot further elicits an ecosystem response.

the context of carrying capacity (Mayer et al., 2006), trophic cascades/ecosystem collapse (Zambrano et al., 2001), and
ecosystem destability (Kilmer and Probert, 1979).
As a whole, the evaluated studies suggest that the magnitude of the ecosystem level response depends on the magnitude
of carrying capacity overshoot (Fig. 2). For example, at a relatively small magnitude of carrying capacity overshoot, a small
magnitude ecosystem responseda small decrease in primary productivity or a small decrease in biodiversitydwould be
expected. However, if the magnitude of carrying capacity overshoot is large enough, a threshold may be crossed and the
ecosystem may change states (Fig. 2). Once in the alternate state, a small magnitude carrying capacity overshoot in the new
state may lead to new additional changes in biodiversity, ecosystem productivity, or elemental cycling, whereas a large
magnitude carrying capacity overshoot may lead to more impactful changes related to ecosystem stability or state changes
(Kilmer and Probert, 1977). Our review of the literaturedparticularly with regards to the implication of carrying capacity
overshootdhighlights the broad application of carrying capacity across research disciplines. The concept often envelopes
disparate and discipline-specific themes under one research area, whether it be population dynamics, biogeochemistry, or
landscape pattern.

5. Conclusions

Given its convoluted history, theoretical elegance, multidisciplinary application, and the variation of application within
each field, it is not surprising that carrying capacity is both widely used and criticized. Carrying capacity is a widely familiar
concept; serial historical applications have given the approach an authoritative influence across disciplines. The concept is
often indiscriminately adopted with little knowledge of why it is used in the discipline. As a result, carrying capacity in-
corporates disparate and fundamental concepts in biology across all levels of ecological organization including, diffusion at
the atomic and cellular level, competition and population dynamics at the population level, available energy and materials at
the ecosystem level, and patches, pattern, and configuration at the landscape level. Nevertheless, there are underlying themes
and similarities with studies that apply carrying capacity.
Though there are several themes and common approaches used in carrying capacity studies that we highlighted in our
study, we argue that uncritical adoption of carrying capacity leads to nonunified applications of the framework. Because the
use and application of carrying capacity is wide-ranging and context specific, we argue that the unifying value of the concept
is lost.
Our review of the application of carrying capacity in ecosystem studies showed that: 1) because of its strong historical ties
to population dynamics, carrying capacity is most often applied at the population leveldcommonly defined as the number of
individuals per unit areadthough there were over a dozen explicit definitions across all levels of ecological organization; 2)
carrying capacity is often considered dynamic with relation to both time and space; 3) carrying capacity is distally controlled
by energy availability and proximally by habitat and food availability; 4) when required resources exceed available resources
there are negative impacts on ecosystems including, a decrease in productivity, biodiversity, and richness, and an increase in
vulnerability to invasion; and 5) there are several links among carrying capacity, ecosystem states, and ecosystem stability.
We end with several suggestions for the application of the carrying capacity concept for future carrying capacity studies.
We argue that future carrying capacity studies should: 1) explicitly state assumptions of a static or variable carrying capacity;
2) use “unpackaged” and deliberate language to explicitly state the particular ecological concepts of the study; 3) frame the
study with fundamental and quantitative ecological principles across all levels of biological organization; and 4) be modified
 E.J. Chapman, C.J. Byron / Global Ecology and Conservation 13 (2018) e00365 9

for the particular application. For example, in shellfish aquaculture studies, fundamentally, the “production carrying capacity”
represents the maximum “sustainable” biomass of shellfish that can be produced without having negative impacts on
phytoplankton and other parts of the food web (e.g. Filgueira et al., 2010; Ibarra et al., 2014) and strongly depends on
ecosystem primary productivity. In this example, framing ecological production of shellfish in terms of universal ecological
concepts such as primary productivity circumvents the linguistic issues of “carrying capacity” while providing a quantitative
assessment of an ecosystem's ability to provide ecosystem services. Furthermore, this particular example highlights the
extent to which carrying capacity is linked to social concepts such as “acceptability” and how “negative impacts” are defined.
By incorporating these suggestions, future ecosystem carrying capacity applications may avoid some of the historical critiques
of the carrying capacity concept.

Acknowledgments

The authors would like to acknowledge funding from the SEES Fellows program (National Science Foundation grant
number: 1313962) and the SEANET project (National Science Foundation grant number: 1355457).

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