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Science of the Total Environment 656 (2019) 789–796

Contents lists available at ScienceDirect

Science of the Total Environment

journal homepage: www.elsevier.com/locate/scitotenv

A nutritional perspective on plastic ingestion in wildlife

Một quan điểm dinh dưỡng về ăn nhựa trong động vật hoang dã

Gabriel E. Machovsky-Capuska a,⁎, Christophe Amiot b, Pablo Denuncio c,


Richard Grainger a,d, David Raubenheimer a,d
a
The University of Sydney, Charles Perkins Centre, Sydney, Australia
b
Université d’Angers, LETG-Angers, LEESA UMR 6554 CNRS, UFR Sciences, France
c
Instituto de Investigaciones Marinas y Costeras, Departamento de Ciencias Marinas, Facultad de Ciencias Exactas y Naturales, Universidad Nacional de Mar del Plata, CONICET, Funes 3350, Mar
del Plata B7602AYL, Argentina
d
The University of Sydney, School of Life and Environmental Sciences, Sydney, Australia

HIGHLIGHTS GRAPHICALABSTRACT

• Our understanding of species' vulnera-


bilities to plastics remains limited
• Nutritional ecology can integrate plas-
tics into broader ecological interactions,
via nutrition.
• We demonstrate how nutritional niches
are tightly linked to plastic ingestion.
• A nutritional framework can enhance
predictions of plastics' impacts on
wildlife.

a r t i c l e in fo abstract

Article history: Although the perils of plastics to living organisms including humans have been neglected for decades, they have
Received 27 September 2018 recently been recognized as a major environmental problem worldwide. Little progress has been made on under-
Received in revised form 26 November 2018 standing the factors that drive species' and populations' susceptibilities to the ingestion of plastic. Here, we pro-
Accepted 27 November 2018
pose using nutritional ecology as a multidisciplinary framework for bridging the gaps that link nutrition,
Available online 28 November 2018
behavior, plastics, physiology and ecology. We show that nutritional niches are tightly linked to plastic ingestion,
illustrating the application of our framework in the context of nutritional niche theory, habitat-specific foraging
Editor: Jay Gan
from species to populations, and transfer patterns in food webs.
Keywords: © 2018 Elsevier B.V. All rights reserved.
Plastics
Multidimensional nutritional niche framework
Pollution
Nutritional goals
Niche theory
Food webs

1. Introduction
E-mail address: g.machovsky@sydney.edu.au (G.E. Machovsky-Capuska).

⁎Corresponding author.
Since the mid-1900s, synthetic organic polymers unlimited range of human activities
known as plastics have been used in a virtually

https://doi.org/10.1016/j.scitotenv.2018.11.418
0048-9697/© 2018 Elsevier B.V. All d.
790 G.E. Machovsky-Capuska et al. / Science of the Total Environment 656 (2019) 789–796

(Thompson et al., 2009). The long-lasting, low cost and lightweight na- foraging behavior (Raubenheimer et al., 2012). Information on how ho-
ture of plastics are key features that have not only made them suitable meostasis engages with different nutritional mixtures helps to predict
for a wide range of products, but also a serious threat to the environ- not only the animal's responses to dietary components that are actively
ment (Derraik, 2002). Within the environment, plastics exist across a targeted in foraging to regulated levels, but also the consequences of
spectrum of different sizes (e.g. mega- (N100 mm), macro- (N20– this regulation for other dietary components that are passively ingested.
100 mm), meso- (5–20 mm) and micro-plastics (b5 mm)) and types For example, numerous studies have shown, both in the lab and the
(e.g. soft packaging including bags, cellophane, bands and hard field, that animals tightly regulate the amounts and balance of energetic
plastics as fragments and pellets) (Derraik, 2002). Although the perils macronutrients (protein, lipids and available carbohydrates) eaten,
of plastic to living organisms including humans have been neglected whereas many (but not all) micronutrients are acquired passively as a
for decades, they have recently been recognized as a major global envi- consequence of macronutrient regulation (Raubenheimer, 2011).
ronmental pollutant affecting terrestrial and aquatic environments as Thus, macronutrient intakes are determined directly by the animal's
well as species across different trophic levels (Barnes et al., 2009; ability, in a given environment, to meet its regulatory targets for these
UNEP, 2011; Wagner and Lambert, 2018). The occurrence and impacts nutrients, whereas micronutrient intakes are determined through cor-
of plastics have been studied almost exclusively in aquatic environ- relations between macronutrient and micronutrient concentrations in
ments, yet the extent and consequences of these pollutants within ter- the foods that are eaten. Central to the message of this paper, is that
restrial ecosystems requires further exploration (Rillig, 2012). There is the predictive power of macronutritional homeostasis can be extended
extensive evidence that plastics are fragmenting in the environment, not only to micronutrients, but also to non-nutritional components,
negatively affecting organisms through entanglement, ingestion (Laist, such as plastics, which might constitute a significant part of the diet
1987, also reviewed in Gall and Thompson, 2015) and the transfer of and yet play no active role in influencing dietary intake.
toxic chemicals (Mato et al., 2001; Teuten et al., 2009). Among marine One tool within the NGF, the right-angled mixture triangle (RMT,
organisms, the ingestion and accumulation of plastics has been mainly Box 1, Fig. 1), models foods and diets as their proportional compositions,
correlated with foraging strategies and diet (Ryan, 1988; Derraik, and thus overcomes the complexities of collecting accurate data on ab-
2002; Bergmann et al., 2015; Nelms et al., 2016; Germanov et al., solute amounts of foods consumed by wild animals in the field
2018). Despite this growing literature, our ability to link diet with plas- (Raubenheimer, 2011). Proportional data modelled in RMTs can be
tic ingestion and its effects predominately concerns marine megafauna gathered from a wide range of sources including gut content analysis
and is often limited to accidentally captured or stranded individuals on (Tait et al., 2014; Denuncio et al., 2017), regurgitations (Hyslop, 1980;
which necropsies can be conducted (Denuncio et al., 2011). Hence, Machovsky-Capuska et al., 2016a, 2018), fecal analysis (Panthi et al.,
there is a great need to enhance and widen our understanding of the 2012) and biologging devices (Machovsky-Capuska et al., 2016b,
general factors and mechanisms that drive species' and populations' 2016d). Detailed discussion of the relative strengths and weaknesses
susceptibilities to the ingestion of plastic (Avery-Gomm et al., 2018). of these techniques is beyond the scope of this paper (reviewed in
Plastic pollution research would benefit from a framework that allows
us to link these susceptibilities with the intricate interactions that
Box 1
occur between individuals and their environment, overcoming current
Right-angled-mixture models (RMT) user's guide.
theoretical and methodological gaps (Rochman et al., 2016). Nutritional
ecology, the field that studies how diet and nutrition link animals with
their environments (Parker, 2003), provides a powerful disciplinary
context for this.
Our goal in this paper is to highlight an approach from nutritional
ecology that can provide a multidisciplinary framework for exploring
links between nutrition, behavior, pollutants, physiology and ecology
(Raubenheimer et al., 2009, 2012). Although these interactions are com-
plex to unravel, the Nutritional Geometry Framework (NGF), offers a
modelling approach to clarify and provide a simplified ecological per-
spective on the key relationships among relevant variables in nutri-
tional ecology (Raubenheimer and Simpson, 1993; Raubenheimer,
2011; Simpson and Raubenheimer, 2012).
In this concepts paper we discuss the use of the NGF to integrate nu-
trition with plastic pollution and illustrate the application of our frame-
work in the context of: 2. Nutritional geometry framework: core i i A B N

concepts, 3. Nutritional and non-nutritional food components, 4. Re-


sponses of animals to plastic ingestion, 5. Quantifying plastics within the
nutritional niche, 6. Nutritional interactions and plastic transfer pat-
terns in food webs.

2. Nutritional geoThetry fraThework: core concepts

Distinguishing features of NGF are that it is multidimensional and


based on the principles of homeostasis (Raubenheimer et al., 2012).
Multidimensionality enables the modelling of nutrition as a set of nested TC TC
Pla
TC

mixtures, from nutrients to foods, meals and diets (Raubenheimer and


Simpson, 2016). This avoids the limiting, and bio- logically unrealistic,
reduction of diet to a single target currency, often assumed to be energy
or nitrogen, rather modelling the core nutritional concept of dietary
balance. The concept of homeostasis introduces a powerful predictive
component in NGF because nutritional homeostasis and its component
mechanisms, such as appetites, underpin much of
G.E. Machovsky-Capuska et al. / Science of the Total Environment 656 (2019) 789–796 791

ways with nutrition and should thus be studied within a nutritional


framework.
One point of interaction with nutrition is through the effect of plas-
tics as a diluent. The mass of plastics consumed ultimately leads to the
displacement of nutritive food in the gut, acting as a nutritional diluent
that can be accumulated in the digestive tract of producers, consumers
and predators over days to years (Bergmann et al., 2015; Provencher
et al., 2017). Since in many animals volumetric feedbacks from stretch
receptors in the gut provide satiety signals to the brain
(Raubenheimer and Simpson, 2018), ingested plastics can thus have
significant negative consequences for nutrient acquisition (Laist, 1987;
Gregory, 2009) and fitness (Ryan, 1988; McCauley and Bjorndal,
1999a). These effects are analogous to the responses of animals ob-
served in a range of studies where individuals have been fed experi-
mentally on foods with differing concentrations of inert nutritional
diluents (reviewed in McCauley and Bjorndal, 1999b; reviewed in
Simpson and Raubenheimer, 2012). Hence, this literature can serve as
a foundation to disentangle the effects of plastic ingestion in animals.
We argue that we should consider plastic pollution to be the unde-
sirable inverse equivalent to nutrition in terms of moderating species'
success. We have identified a two step-process that must be achieved
to understand how plastics shape nutritional and ecological interac-
Fig. 1. Right-angled mixture triangle (RMT) showing hypothetical foods (black hollow
circles) that contain different proportions of P, L and Pla as follows: (i) 40% P, 40% L and tions. First, to understand the real physiological, ecological and behav-
20% Pla; (ii) 0% P, 0% L and 100% Pla and (iii) 50% P, 10% L and 40% Pla. The model also ioral influence of plastics in animals, we should include them in the
illustrates that if an animal mixes its intake of two foods (e.g., i and iii), the resulting definition of “nutrients” proposed by Westoby (1978), as “any property
diet composition is constrained to lie on the line connecting the foods (e.g., black solid
of a food which affects how it benefits the animal”. Thus, foods should
star). By mixing its intake of three foods (e.g., i, ii, and iii), the accessible space expands
to a triangle connecting these foods (e.g., black hollow star). The nutritional niche of the be considered in future studies as complex mixtures of nutrients and
species is constrained to lie on the black dashed line connecting the dots. often plastics (in micro and macro sizes) with different fitness implica-
tions to the forager. Second, a standardized use of mass of plastic
ingested as a metric in reporting protocols can foster the integration
Majdi et al., 2018). However, the combination of multiple approaches of ecological principles (Rochman et al., 2016; Provencher et al., 2017).
can overcome the shortfalls of each one alone and improve our esti- Recently, the NGF provided the basis for the development of a mul-
mates of diets (Munafò and Smith, 2018) and plastic ingestion. tidimensional nutritional niche framework (MNNF) for integrating nu-
RMTs have been increasingly used to address questions in field- trition with ecological niche theory to better understand and
based nutritional ecology from individuals to populations and species characterize the concept of dietary generalism (Machovsky-Capuska
(Tait et al., 2014; Raubenheimer et al., 2015), applied to micro- and et al., 2016c). MNNF has the advantage of offering four functional levels
macronutrients, and pollutants (Raubenheimer et al., 2012; Nie et al., to define the nutritional niche of a species: the fundamental nutritional
2014) within marine (Tait et al., 2014; Machovsky-Capuska et al., niche breadth (the dietary macronutrient compositions on which a pop-
2016b) and terrestrial environments (Rothman et al., 2011; ulation is physiologically able to persist and thrive), the realized nutri-
Raubenheimer et al., 2015). This approach has contributed significantly tional niche breadth (the macronutrient compositions of diets that can
to the study of animal nutrition in the wild across several research dis- sustain a population given ecological constraints, e.g. environmental
ciplines including wildlife conservation (Rothman et al., 2011; fluctuations, human pressures), the food composition niche breadth
Raubenheimer et al., 2015; Denuncio et al., 2017), movement ecology (the range of food compositions that can be exploited to compose the
(Nie et al., 2014), human-wildlife interactions (Coogan and diet) and the food exploitation niche breadth (the range of ecological
Raubenheimer, 2016) and urban ecology (Machovsky-Capuska et al., and physical attributes of foods that a population is able to exploit).
2015; Coogan et al., 2017, 2018), as well as to human nutrition The inclusion of plastics within a proportional-based integrated
(Raubenheimer and Simpson, 2016). modelling framework (MNNF) will enhance our understanding of
how plastic ingestion interacts with food and nutrient intakes of ani-
mals across ecological contexts. This is important if we are to predict
3. Nutritional and non-nutritional food coThponents how species will respond to environments with different plastic con-
centrations. Mixtures of nutrients and plastics are modelled from a
The ecology and the evolution of animal life-history traits are wide range of foods, which combined could allow us to unravel the in-
strongly influenced by diet (Pascacio-Villafán et al., 2016). While mac- tricate interactions between them across different meals and ultimately
ronutrients (protein, carbohydrate, and lipid) can explain a good deal of the diets of individuals, populations and species (Fig. 1 in Box 1).
the variation in the behavioral, physiological and performance re-
sponses of animals (Simpson and Raubenheimer, 2012), micronutrients 4. Responses of aniThals to plastic ingestion
and non-nutritional food components, such as chitin, bones, hair, oto-
liths and plant secondary metabolites are also important (Jobling and A wide range of organisms ingest plastics either actively (e.g. active
Breiby, 1986; DeGabriel et al., 2014). feeding) or passively (e.g. sifting through sediments, filtering water or
In recent decades, anthropogenic activities have led to the introduc- through the consumption of foods that contain plastics within their tis-
tion of chemical and physical pollutants into the environment on an un- sues) (Wright et al., 2013). Marine vertebrates are known to actively feed
precedented scale. Contamination of habitats and organisms by plastics, on plastics of different types, sizes, buoyancy and colors (Derraik,
in particular, is now globally ubiquitous with no signs of abatement 2002). Mistaken identity due to similarities in the characteristics of plas-
(Rochman et al., 2016). Plastics can be passively and actively consumed tics with natural prey (e.g. gelatinous prey, fish eggs, plankton, poly-
by organisms, and thus represent a new addition to ecological food chaetes) is the general explanation for active consumption of plastics
webs. Although not nutritional, plastics can interact in fundamental (Mattlin and Cawthorn, 1986; Laist, 1987; Miranda and de Carvalho-
792 G.E. Machovsky-Capuska et al. / Science of the Total Environment 656 (2019) 789–796

Souza, 2016; Savoca et al., 2017; Würsig et al., 2017). However, the nu- Table 1
Outstanding research questions that emerge from integrating plastic ingestion to nutri-
tritional consequences of these decisions remain to be established.
tional ecology.
An important challenge ahead is to use a multidimensional frame-
work to explore foraging decisions in species that are prone to passive Responses of animals to plastic ingestion
ingestion of plastics. Ecologists have gathered overwhelming evidence ➢ Are nutritional generalists more prone to consume and accumulate plastics
than specialists?
on the passive ingestion of microplastics by filter-feeders (barnacles,
➢ What are the nutritional, physiological and fitness consequences of species
whales), detritivores (amphipods) and carnivores (fish, seabirds, mam- that passively and actively consume plastics?
mals, sharks, reptiles) (Thompson et al., 2004; Dantas et al., 2013, 2015; ➢ How might foragers respond to the consumption of plastics and foods that are
Ramos et al., 2012; Bonanno and Orlando-Bonaca, 2018). Microplastics nutritionally diluted by them?
can be passively ingested through water, sediments or foods (Cole et Linking habitat-specific foraging, nutritional niche and plastic ingestion
➢ How do plastic polluted environments influence the populations of nutritional
al., 2011). Particularly important is the question of whether and how generalists and specialists?
the foraging and feeding patterns of animals respond to plastics in the ➢ What are the nutritional decisions of individuals foraging in plastic polluted
foods they eat. and clean habitats?
Organisms, from slime molds to vertebrates, can solve complex nu- Nutritional interactions and plastic transfer patterns in food webs
tritional challenges according to their current or future nutritional re- ➢ How might food webs respond to plastic pollution?
➢ Does plastic ingestion shape foraging decisions and nutritional intake within
quirements (Dussutour et al., 2010; Simpson et al., 2010). In theory, a
trophic levels?
forager could adjust its feeding behavior to avoid foods that are nutri- ➢ To what extent plastic ingestion in producers (e.g. plankton) influences inter-
tionally diluted by plastics. Genes, hormonal signals and nutrient- actions at higher trophic levels?
sensing mechanisms will assess the nutritional state of an organism to
determine any potential nutritional deficits (Ren et al., 2009). Animals
may thus compensate for nutrient dilution by plastics by increasing the inevitable heterogeneity in both the methods and aims of studies,
their food intake to meet specific nutrient needs (Simpson and they also provide the opportunity to integrate data across spatiotempo-
Simpson, 1990). If there is asymmetry in the distribution of plastics in ral scales that would not be feasible in any one study (Remonti et al.,
foods of different compositions (for example, if fatter animals store 2015).
more plastic than leaner ones), it is even possible that plastics might in- Given the large range of feeding strategies and forms of plastic that
fluence the intakes of some nutrients more than others, thus skewing occur within the environment, work is needed to explore whether plas-
the balance of nutrients eaten. Alternatively, these effects may be over- tic types shape the nutritional niche breadths of species and popula-
ridden by the strong nutrient balancing mechanisms that have been ob- tions. To illustrate (Fig. 2), following Machovsky-Capuska et al. (2018),
served across a wide range of animals (Simpson and Raubenheimer, we combined MNNF with standard ellipse areas corrected for small
2012). Among these is nutritional-state-dependent learning which has sample sizes (SEAc) on stomach content data extracted from
been related to positive associations (e.g. food cues or locations), aver- Denuncio et al. (2011, 2017). We compare the minimal range of dietary
sions (e.g. nutritionally poor or toxic foods and quality of foraging hab- compositions that contributes to the nutritional niche breadths of 26
itats) and non-associative responses (e.g. adjust foraging strategies or
find novel foods when needed) (Simpson and Raubenheimer, 1996;
Berthoud et al., 2012). Likewise, nutrient-specific appetites might en-
able animals to increase their intake of specific foods allowing them to
achieve the required dietary nutrient balance despite differential dilu-
tion of particular nutrients by plastics (Raubenheimer and Simpson,
2018).
An important area of future research is to expand upon field- and
experimental-based nutritional ecology studies to link the nutritional
effects of plastic intake to biological responses (e.g. immunity, repro-
duction and lifespan). This approach could provide valuable insight
into the range of foods that a species can exploit, improving our esti-
mates of the food composition niche and measure the realized nutri-
tional niche to better estimate the diet of a population under
ecological constraints (Machovsky-Capuska et al., 2016c) (Fig. 1). This
will certainly inspire broader ecological questions (see Outstanding re-
search questions in Table 1).

5. Quantifying plastics within the nutritional niche

Little progress has been made in linking the influence of plastic pol-
lution with foraging behavior and habitat use (Ryan, 1987, 1988; Young
et al., 2009; Fukuoka et al., 2016). Despite the wealth of available infor-
mation, there are several non-exclusive plausible contributing factors.
First, there is a growing consensus that we lack a common framework
for addressing such questions (Rochman et al., 2016; Provencher et al.,
Fig. 2. Right-angled mixture triangle (RMT) showing the influence of type of plastics and
2017; Avery-Gomm et al., 2018). Second, the problem also extends to
niche breadth of 26 Franciscana dolphins contaminated by this pollutant. Each point
the belief that properly designed large-scale field studies are needed to represents the stomach content proportional composition of protein (P), lipid (L) and
provide insights into the ecological impacts of contaminants in differ- ent Water (W) of individual dolphins. Following Machovsky-Capuska et al. (2018), the
habitats (Browne et al., 2015). Third, a high inter-individual variabil- ity minimal realized nutritional niches are measured as the area of standard ellipse (SEAc).
in responses of organisms to contaminants hampers the translation of Dolphins that consumed hard plastics (hollow triangles, SEAc: 15.24, dark grey dashed
ellipse), dolphins that consumed packaging plastics (hollow squares, SEAc: 13.66, black
risks and impacts up to populations (Stark et al., 2004). Coupling
dashed dot ellipse), and dolphins that consumed both type of plastics (hollow circles,
MNNF with data from literature is a first step for bridging this gap. Al- SEAc: 6.23, grey dashed dot ellipse)
though secondary analyses of published data have limitations due to (Data from Denuncio et al. 2011 and 2017).
G.E. Machovsky-Capuska et al. / Science of the Total Environment 656 (2019) 789–796 793

Franciscana dolphins (Pontoporia blainvillei) from Argentina that con-


sumed hard plastics (e.g. fragments, pellets) and packaging plastics
(e.g. cellophane bands, bags). The comparison suggests that dolphins
had different realized nutritional niche breadths and wet mass
protein-to-lipid ratios (P:L) depending on whether they ingested hard
plastics (SEAc: 15.24, P:L from 2.87 to 15.47), soft plastic packaging
(SEAc: 13.66, P:L from 3.56 to 11.02) and consumed both soft packaging
and hard plastics (SEAc: 6.23, P:L from 4.78 to 27.71). SEAc analysis pro-
vides the best estimate for studies with small samples (Syväranta et al.,
2013), albeit with limitations. Although we acknowledge the challenges
of collecting reliable data that combines plastic and food ingested pro-
portions, and the nutritional composition of foods, studies with increas-
ing samples sizes will certainly provide robust conclusions about the
influence of plastics in nutritional niches. A starting point could be to
further explore the effects of the accumulation of natural, indigestible
components in the stomach (e.g. chitin exoskeletons; cephalopod
beaks) that are linked to food preferences in foragers. This in turn can
provide potential explanations of how different categories of plastics
shape nutritional niches among species.
Unfortunately, very few studies have presented evidence linking the
ecological effects of plastics to the wildlife populations that inhabit an
environment (Browne et al., 2015). Young et al. (2009) used GPS logger
on Laysan albatross (Phoebastria immutabilis) and found that individ-
uals foraging in plastic polluted regions brought back more plastic to
their chicks than those foraging in less polluted environments. A reduc- Fig. 3. Right-angled mixture triangle (RMT) showing the realized nutritional niche
tion or shift in the range of achievable dietary nutritional compositions breadths including plastics of 24 Franciscana dolphins that ingested plastics from
due to plastics could impact on the ability of individuals to meet their estuarine (grey triangles) and marine (black hollow circles) habitats. Each point
represents the stomach content proportional composition of protein (P), lipid (L) and
nutritional goals, with implications for their populations (Machovsky-
plastic (Pla) of individual dolphins. Following Machovsky-Capuska et al. (2018), the
Capuska et al., 2016c). To illustrate, we linked proportional data on plas- minimal realized nutritional niches are measured as the area of standard ellipse (SEAc).
tic ingestion with the MNNF to explore potential nutritional responses Estuarine dolphins SEAc: 75.81, grey ellipse and marine dolphins SEAc: 27.43, black ellipse
of two different sub-populations from the most threatened small ceta- (Data from Denuncio et al. 2011 and 2017).
cean in the western South Atlantic Ocean, the Franciscana dolphin
(Crespo et al., 2010). From a published dataset extracted from Nutriscapes combined with plastic pollution surveys have the potential
Denuncio et al. (2011, 2017), we only used individuals that consumed to provide: i) novel estimates of how much plastic (including type, size,
plastics. The former study concluded that dolphins from marine and es- volume, mass) is encountered by organisms in different habitats; ii) ex-
tuarine environments ingested different proportions of plastics, amine the foraging trade-offs between nutrients and plastics in polluted
whereas the latter suggested that sub-populations from different habi- and clean environments; iii) an integrated ecological risk assessment of
tats consumed diverse nutritional compositions of prey (Denuncio et the extent of the impacts of plastics in habitats.
al., 2017). Significantly more plastic was ingested in estuarine habi-
tats than in marine habitats (LM, F1,24 = 6.24, P b 0.05). Fig. 3 illustrates 6. Nutritional interactions and plastic transfer patterns in food webs
habitat differences in the minimal realized niche breadths between es-
tuarine (SEAc: 75.81, wet mass P:L from 2.38 to 15.50) and marine dol- Plastics of different sizes, colors and types can be consumed among
phins (SEAc: 27.43, P:L 2.38 to 13.90). Although far more reliable results different trophic levels in marine and freshwater coastlines and open
can be obtained with greater sample sizes, the comparison does show waters, within the surface, the depths and the floors (Laist, 1987; Avio et
that even data extracted from the literature that includes plastic inges- al., 2017; Savoca et al., 2017). Inconspicuous microplastics have been
tion and nutritional intakes from different habitats can be used to infer identified as ubiquitous components of all marine trophic levels,
nutritional priorities of different species and populations under diverse spreading through either direct or indirect consumption (Wright et al.,
ecological constraints. 2013; Chae and An, 2017). Poor understanding of the ability of marine
Physico-chemical characteristics of estuarine ecoclines can influence organisms to digest, break down or egest microplastics from their bod- ies
the estuaries' efficiency to trap plastics, with a greater likelihood of in- (Wright et al., 2013), combined with concerns regarding their poten- tial
gestion of microplastics by organisms inhabiting estuaries than the av- toxicity leads to a serious environmental problem (Chae and An, 2017).
erage in coastal and marine settings (Barletta et al., 2019). This Public health concerns could also be raised when the species are
general trend is likely to impact the ability of individuals within a pop- important for human consumption (Miranda and de Carvalho- Souza,
ulation to reach their nutritional goals, influencing the breadth of the re- 2016; Smith et al., 2018).
alized nutritional niche (Machovsky-Capuska et al., 2018). The inclusion It has been recognized that our efforts to understand the ecological
of anthropogenic pressures (e.g. plastic pollution) in nutritional niches, interactions of plastics and nutrients within trophic webs lack a rigorous
provides a comprehensive representation of the ecological constrains and consistent approach (Derraik, 2002; Rochman et al., 2013;
that are critical to species' and populations' nutrition and fitness Provencher et al., 2017). Compelling evidence suggests that
(Machovsky-Capuska et al., 2016c). microplastics are often introduced into the food web through initial in-
Spatial and temporal patterns in the amounts of plastics and how gestion by producers (e.g. plankton) and low-level consumers (e.g.
frequently individuals are exposed to them are poorly understood crustaceans, bivalves) which are subsequently preyed on by predators
(Browne et al., 2015). Nutritional landscapes (nutriscapes) can provide (e.g. fish and cephalopods) and then larger apex predators (e.g. sea-
a unique opportunity to reconstruct foraging behaviors and habitat use birds, sharks, predatory fish, marine mammals) (reviewed in Miranda
linked with geographic location, abiotic factors (e.g. sea surface temper- and de Carvalho-Souza, 2016). Trophic level relationships within food
ature, and bathymetry) and temporal measures of resource acquisition webs are mainly a function of nutritional benefits to different predators
quantified as specific nutrients (Machovsky-Capuska et al., 2018). (Hastings and Conrad, 1979; Raubenheimer et al., 2009; Wilder et al.,
794 G.E. Machovsky-Capuska et al. / Science of the Total Environment 656 (2019) 789–796

2013). Therefore, linking nutrition with plastic ingestion seems crucial if multidisciplinary lines of research (see Outstanding Questions in Table
we want to unravel the paths of these pollutants throughout trophic 1). We hope that researchers will be encouraged to incorporate this
levels. framework to move beyond isolated descriptions and integrate plastics
In Fig. 4, we show different scenarios for nutrient and plastic interac- into a broader nutritional and trophic context, which can help to direct
tions in the context of food webs. As trophic levels increase, body com- future research and unify the existent literature.
positions will have higher protein to lipid ratios due to homeostatic
feeding and growth responses (Raubenheimer et al., 2009). Therefore,
AcknowledgeThents
consumers become lipid limited with increasing trophic level, providing
a nutritional incentive to feed down the food web, on prey with a lower
We thank Samantha M. Solon-Biet for constructive comments on an
P:L content. Additionally, the regulation of lipid and protein intake by
earlier draft. We also thank the anonymous reviewers that helped to im-
predators could encourage individuals to feed across multiple trophic
prove this manuscript.
levels and thus different protein-to-lipid ratios (Wilder et al., 2013).
Thus, depending on the trophic level at which a consumer is feeding
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