# Construction costs and tradeoffs in carnivorous pitcher plant leaves: towards a pitcher leaf economic spectrum

Kadeem Gilbert, David Armitage, Ulrike Bauer, Kenji Fukushima, Laurence Gaume, Rachel Love, Qianshi Lin, Sukuan Liu, Sylvie Martin-Eberhardt, Jonathan Millett, et al.

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## To cite this version:

Kadeem Gilbert, David Armitage, Ulrike Bauer, Kenji Fukushima, Laurence Gaume, et al., Construction costs and tradeoffs in carnivorous pitcher plant leaves: towards a pitcher leaf economic spectrum. Annals of Botany, 2025, 135 (7), pp.1261-1279. 10.1093/aob/mcaf024. hal-04989040

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INVITED REVIEW

# Construction costs and tradeoffs in carnivorous pitcher plant leaves: towards a pitcher leaf economics spectrum

Kadeem J. Gilbert<fnref n="1" />,*, David Armitage², Ulrike Bauer³, Kenji Fukushima⁴, Laurence Gaume⁵,
Rachel Love⁶, Qianshi Lin⁷, Sukuan Liu⁸,⁹, Sylvie Martin-Eberhardt<fnref n="1" />, Jonathan Millett¹⁰,
Tanya Renner⁷, Mathias Scharmann¹¹ and Chris Thorogood¹²,¹³

Received: 4 December 2024

Returned for revision: 18 February 2025

Editorial decision: 25 February 2025

Accepted: 23 March 2025

* **Background** Leaf economics theory holds that physiological constraints to photosynthesis have a role in the coordinated evolution of multiple leaf traits, an idea that can be extended to carnivorous plants occupying a particular trait space that is constrained by key costs and benefits. Pitcher traps are modified leaves that may face steep photosynthetic costs: a high-volume, three-dimensional tubular structure may be less efficient than a flat lamina. While past research has investigated the photosynthetic costs of pitchers, the exact suite of constraints shaping pitcher trait variation remain under-explored, including constraints to carnivorous function.

* **Scope** In this review, we describe various constraints arising from the dual photosynthetic and carnivorous functions of pitchers arising from developmental, functional, budgetary and environmental factors. In addition, we identify the data required to establish the leaf economics spectrum (LES) for carnivorous pitcher plants (CPPs), and – owing to the multifunctional roles of pitcher leaves – discuss difficulties in placing pitchers onto existing frameworks.

* **Conclusion** Because pitcher traps serve multiple functions, both photosynthesis and nutrient acquisition (carnivory), they are difficult to place in the context of the LES, especially in light of a current lack of trait data. We describe a spectrum across the independent CPP lineages in approaches to balancing carnivory–photosynthesis tradeoffs. Future efforts to collect relevant data can clarify the forces that shape observed pitcher trait variation, and increase understanding of principles that may be ultimately generalized to other plants.

**Key words:** Carnivorous plants, pitcher plants, leaf economic spectrum, *Cephalotus*, *Nepenthes*, *Sarracenia*, *Heliamphora*, *Darlingtonia*.

INTRODUCTION

The leaf economics spectrum (LES) is a conceptual framework that has advanced knowledge of the correlations among leaf traits, clarified environmental correlates of these traits, and revealed tradeoffs in leaf construction by way of constraints over nutrient and energy allocation (Wright et al., 2004). This framework focuses on a few key functional traits that can be measured in a standardized way across the global diversity of leaves.

Doing so de-emphasizes the idiosyncrasies of specific lineages to identify the general factors constraining the geographical, environmental and phylogenetic distributions of traits. For instance, shorter-lived leaves tend to invest highly in photosynthesis and nutrient acquisition at the expense of leaf mass per unit area (LMA), in contrast to longer-lived leaves. This tradeoff is predicted to be because the balance of the costs and benefits of increased LMA has a longer payback-time than a

<footnote n="1">¹W.K. Kellogg Biological Station, Department of Plant Biology, and Program in Ecology, Evolution & Behavior, Michigan State University, Hickory Corners, MI, USA, ²Integrative Community Ecology Unit, Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha, Onna-son, Kunigami-gun, Okinawa, Japan, ³Department of Biosciences, University of Exeter, Geoffrey Pope Building, Stocker Road, Exeter, UK, ⁴Center for Frontier Research, National Institute of Genetics, 1111 Yata, Mishima, Shizuoka 411-8540, Japan, ⁵AMAP, Montpellier University, CNRS, CIRAD, INRAE, IRD, Montpellier, France, ⁶Learning Commons, Kalamazoo College, 1200 Academy Street, Kalamazoo, MI, USA, ⁷Department of Entomology, The Pennsylvania State University, 501 Agricultural Sciences and Industries Building, University Park, PA, USA, ⁸Department of Biology, Colorado State University, 251 W Pitkin St, Fort Collins, CO 80521, USA, ⁹Department of Ecology and Evolutionary Biology, University of Colorado Boulder, 1900 Pleasant Street, Boulder, CO 80309, USA, ¹⁰Department of Geography & Environment, Loughborough University, Epinal Way, Loughborough, LE2 1YE, Leicestershire, UK, ¹¹Institute for Biochemistry and Biology, Genetics Research Group, University of Potsdam, Building 26, Room 1.50, Karl-Liebknecht-Str. 24-25, 14476 Potsdam, Germany, ¹²Botanic Garden, University of Oxford, Rose Lane, Oxford, OX1 4AZ, UK and ¹³Department of Biology, University of Oxford, Zoology Research and Administration Building, 11a Mansfield Rd, Oxford OX1 3SZ, UK</footnote>

<footnote>*For correspondence. E-mail gilbe334@msu.edu</footnote>
short leaf lifespan allows. Because leaves are costly in terms of
nutrient use, the key environmental controls over variability are
found across light and nutrient gradients. In sunny conditions,
thicker leaves with higher nitrogen concentrations are more ef-
fective at intercepting light; shade leaves tend to be thinner with
lower nitrogen concentrations. In nutrient-replete conditions,
short-lived leaves with low LMA and high N concentrations are
more effective at fast growth in a competitive environment; in
nutrient-poor conditions, long-lived leaves with high LMA and
low N concentrations use the limited nutrient resource more
conservatively. The utility of this trait-based framework has
been extended in consideration of other tissues and organs as
well, including wood (Chave et al., 2009), roots (de la Riva et
al., 2021) and flowers (Roddy et al., 2021). One major know-
ledge gap concerns the tradeoffs involved in multi-function
plant structures, such as those required for both carbon fixation
and nutrient or water acquisition, for example the photosyn-
thetic roots of epiphytic orchids and the prey-trapping struc-
tures of carnivorous plants (CPs) – the latter of which are the
focus of this review.

Plant carnivory is a habit defined by multiple components,
including adaptations for the attraction, capture, retention, di-
gestion and assimilation of nutrients derived from animal prey.
Carnivorous plants have evolved multiple times independently:
at least ten origins within Angiosperms, over 800 total species
(Ellison and Adamec, 2018). This has been linked to the se-
lective pressures of nutrient-limited environments (Givnish et
al., 1984). The leaves of this group of plants function as traps
for catching and digesting arthropods, but the traits of carniv-
orous leaves are themselves very variable, comprising multiple
distinct trapping strategies including snap traps, sticky traps
and pitcher traps, among others (Ellison and Adamec, 2018).
The need to function as a trap means that CP leaves may fall
outside the range of variation for more ‘typical’ leaves, espe-
cially in pitcher plants. Additionally, it is interesting to contem-
plate why carnivory overall comprises such a wide variety of
strategies, while other plant functions may be relatively more
constrained. Considering specifically pitfall traps, this strategy
is relatively rare amongst land plants [~200 pitcher plant spe-
cies, ~837 CPs in total (Ellison and Adamec, 2018); see Box
1], and species employing this trait tend to be patchily distrib-
uted and most abundant in remote regions that can be difficult
to access. Furthermore, it is often unclear how some canonical
plant leaf traits are measured on such complex, 3-D structures.
For these reasons, pitcher plants are not commonly included in
large-scale trait-based studies (Box 2), yet the atypical traits of
pitchers could serve as a key for a more comprehensive, global
view of the LES.

There are many reasons why pitcher plants represent an
interesting extension of the LES. As the currency of the LES
is carbon produced by photosynthesis, leaves tend to be rela-
tively flat because a high surface-to-volume ratio is the most
efficient form for photon capture. Thus, the high-volume, 3-D,
tubular leaf structure of pitcher plants represents an extreme
deviation from photosynthetic efficiency. Therefore, a first
key question is whether the LES model is suitable for pitcher
leaves to begin with. Moreover, pitcher plants are of interest
because they separate photosynthesis and nutrient acquisition
both temporally and spatially: for example, *Cephalotus* leaves
shift between these functions through time (depending on con-
ditions), while *Nepenthes* leaves comprise a 3-D pitcher for

prey capture, together with a 2-D lamina for photosynthesis,
as we discuss below. Beyond their 3-D architecture, pitchers
are also multi-role organs (though this role may be reduced in
*Nepenthes* pitchers) that must capture light and also function
as ‘above-ground roots’ to acquire growth-limiting nutrients
such as nitrogen and phosphorus. This extreme alteration of
the photosynthetic structure may also explain the widely re-
ported gene loss in their plastid genomes, perhaps suggesting
a downsizing of photosynthetic function at a molecular level
(Wicke et al., 2014; Ross et al., 2016; Fu et al., 2023; Silva
et al., 2023). From what has been measured thus far, pitcher
plants tend to have low photosynthetic rates (A_N), and may have
atypically high rates of dark respiration (R) due to their un-
usually high levels of alternative oxidase (Pavlovič and Kocáb,
2022). An in-depth exploration of pitcher traits considering the
particular set of functions the plants must achieve can reveal
novel ways of applying the LES, or even expand our view of
the broader total trait space onto which leaves can fall. At one
level, the LES can be a tool to understand the vast variation
in pitcher size and morphology observed in nature; at another
level, incorporating pitchers into the LES opens up the oppor-
tunity to test the general validity of the LES for other highly
modified leaves (succulent leaves, tendrils, spines, etc.).

The LES is, by definition, a framework for understanding
covariances between leaf traits and relating these covariances
to developmental, functional, ecological or evolutionary fac-
tors. To provide insight on pitcher trait space, we have chosen
to focus on four potential constraints to the evolution of trait
variance within this group: (1) developmental constraints, i.e.
the mechanisms responsible for the production of pitcher plant
morphologies; (2) functional constraints, i.e. the adaptive ends
to variation in these structures/traits; (3) budgetary constraints,
i.e. constraints due to a major functional tradeoff observed in
this group and differential allocation to either function; and
(4) environmental constraints, i.e. how abiotic factors may
further shape their trait distribution. These four angles repre-
sent major axes that can be applied to diverse plant groups.
Further, we specifically investigate each constraint in relation
to two major functional categories pitcher leaves must achieve:
photosynthetic and carnivorous functions. Recognition of the
specific importance of both of these functional categories (and
the tradeoffs between them) to pitcher plants is a major motiv-
ator for exploring this proposed framework. In the following
sections, we present evidence – where available – and interpret-
ations on the existence of trait variation and potential covari-
ances or tradeoffs at each of these biological constraints. In a
sense, these constraints can be envisioned as a series of filters
from what is theoretically possible to that which is evolution-
arily feasible and phenotypically realized. In considering which
traits to measure and the potential factors constraining them, we
also outline important, unanswered questions that only coord-
inated, trait-based approaches can address, which we hope will
motivate additional research on pitcher plant traits and enable
an LES analogue for these multi-function plant structures.

DEVELOPMENTAL CONSTRAINTS ON
PHOTOSYNTHESIS

Carnivorous plants face the unique challenge of balancing two
primary functions within a single organ: photosynthesis and
## BOX 1. COMPARISON OF DIFFERENT LINEAGES OF CARNIVOROUS PITCHER PLANTS

The pitcher is one of a handful of divergent trapping structures that have evolved among carnivorous plants. In pitcher plants, the leaf has been modified into a tube-shaped pitfall trap. Insects attracted to the pitcher land on slippery rims which causes them to fall into a pool of digestive fluid. This strategy has evolved at least three times independently, in the families Sarraciaceae (Ericales), Nepenthaceae (Caryophyllales) and Cephalotaceae (Oxalidales). In a broader sense, the pitfall strategy also applies to a handful of carnivorous bromeliad species (Brocchinia reducta, B. hectioides, Catopsis berteroniana) and the potentially carnivorous Paepalanthus bromelioides (Eriocaulaceae), also in the Poales. However, unlike in the case of pitcher plants sensu stricto, these pitfall traps consist of tanks created by multiple tightly overlapping leaves. In Sarraciaceae, Nepenthaceae and Cephalotaceae, pitcher traps are all formed by individual leaves. These 'true pitcher plants' have many similarities in the general structure of their pitchers, including a lid covering the trap opening (the operculum), a slippery rim (the peristome), the tubular pitcher body with a slippery inner wall and the glandular digestive zone at the bottom of the inner pitcher wall, which also contains the digestive fluid.

The pitcher plants sensu lato in Bromeliaceae and Eriocaulaceae create fluid-filled tanks with multiple closely appressed leaves. By examining these multi-leaved pitcher plants, we can still test the extent to which the LES applies to carnivorous pitcher plants. While developmental constraints of single-leaved pitchers are probably already low, the developmental constraints of creating a tank bromeliad pitcher may be even lower, as it requires no rolled leaf. However, the functional requirement to attract, trap and digest prey, as well as to convert carbon to sugar, remains. Although each individual leaf does not function as a pitcher, the individual leaves are still governed by functional constraints on the entire pitcher's ability to catch prey. For example, individual leaves produce a crumbling wax layer on the inner wall that interferes with adhesion between insect feet and the pitcher surface (Gaume et al., 2004; Nishi et al., 2012). In contrast to single-leaved pitchers, there is likely to be between-leaf variability in leaf photosynthetic efficiency; those forming the tank are quite vertical, reducing photosynthetic efficiency, but outer leaves are at a more typical angle for bromeliads and should have a more typical photosynthetic contribution to the plant. Thus, the net cost of each leaf is probably more variable in multi-leaved pitchers than in single-leaved species. Here we hypothesize similar functional constraints between single-leaved and multi-leaved pitchers, lower developmental constraints in multi-leaved pitchers, and budgetary constraints are more variable. Examining the various constraints on each leaf of a carnivorous bromeliad would test the limits of the LES.

carnivory. As a response, some lineages, such as Nepenthes, spatially partition these functions: the distal portion of the leaf

## BOX 2. PITCHER TRAITS IN LARGE-SCALE PLANT TRAIT DATABASES

Large-scale collaborative databasing efforts have potentiated a move toward trait-based ecology in the past two decades, which has provided new insights into ecosystem processes, trait evolution and plant function. These databases provide free access to trait data allowing for a diversity of large-scale studies that seek to describe and explain the vast trait variation found globally. One example of such a plant trait database is TRY (Kattge et al., 2020), which is one particularly large and comprehensive database. As of the time of access, TRY contains 15 409 681 trait records from 305 594 species. This is a massive amount of data, but there are still gaps in our knowledge. One major gap concerns the tradeoffs involved in multi-function plant structures, such as those required for both carbon fixation and nutrient or water acquisition, for example the photosynthetic roots of epiphytic orchids or the prey trapping structures of carnivorous plants – the latter of which are the focus of this review.

To examine the state of trait data for these plants, we downloaded the data for all available pitcher plant species in the TRY database (Kattge et al., 2020); this yielded 135 species with a total of 143 available traits. In contrast, if a random subset of 135 non-carnivorous species is selected, its trait table yields an average of 418 total measured traits (Supplementary Data). This illustrates that, even considering the relatively small number of species, pitcher plants have not been subject to the same depth and breadth of trait measurements, relative to non-carnivorous plants within this database. Compared to other plant groups, either fewer traits have been recorded and uploaded for pitcher plants, and/or researchers have yet to determine a standardized set of trait measurements that would facilitate ease of entry into large databases. Consequently, cross-species trait comparisons are less frequent within pitcher plants as a group. This is surprising, given that leaf and pitcher trap trait variation in these clades can be very high and are often used for species delimitation. This presents an opportunity for a more consistent trait-based approach to pitcher plant biology, expanding our database of traits to better-understand these evolutionary enigmas, and how they fit into the existing framework.

in Nepenthes forms a pitcher to capture prey, while the proximal portion is flattened and oriented optimally for photosynthesis. This division utilizes the inherent segmentation found in most flowering plant leaves, which typically consist of three parts: the leaf blade, the petiole and the leaf base (Franck, 1976). In pitcher plants, either the leaf blade itself develops into a trap, or traps emerge from apical tendrils extending from the blade. In some Nepenthes species, trapping pitchers have almost no photosynthetic activity, indicating a high degree of functional compartmentalization and specialization (Pavlovič et al., 2007; Capó-Bauçà et al., 2020). The tendril in this genus can also have an important climbing and support function. The leaf base, including stipules, can contribute to photosynthesis in some
flowering plant lineages and forms the flat, photosynthetic por-
tion of Nepenthes leaves.

While Nepenthes uses a compartmentalized leaf organiza-
tion, Cephalotus is phenotypically plastic, showing a shift in
leaf type depending on environmental conditions. For example,
in a controlled environment, Cephalotus generates photosyn-
thetic leaves at 15 °C and carnivorous leaves at 25 °C. This
shift aligns with the seasonal temperature variations of natural
habitats and possibly correlates with the likelihood of capturing
prey. Occasionally, these plants may produce leaves that are
neither fully photosynthetic nor fully carnivorous (Fukushima
et al., 2021), adding another layer of complexity to the adap-
tive benefits and costs of leaf development. Sarracenia utilizes
a hybrid approach, combining leaf segmentation with pheno-
typic plasticity to optimize both photosynthesis and carnivory
(Ellison and Gotelli, 2002).

DEVELOPMENTAL CONSTRAINTS ON CARNIVORY

Once leaves have evolved to form pitcher traps, there are still
a number of structural or developmental factors constraining
their overall morphological breadth. In *Heliamphora*, the mor-
phological evolution of adult pitchers was found to be struc-
turally constrained, as indicated by the strong evolutionary
correlations between pitcher shape variations (i.e. pitcher stout-
ness and curvature) and maximum pitcher size (length) (Liu
and Smith, 2023). *Heliamphora* species with slender or straight
pitcher shapes are associated with larger pitcher sizes, while
taxa with stout or curved pitcher morphologies correlate with
smaller pitcher sizes. Liu and Smith (2023) postulated that
stout or curvy pitchers are less structurally stable compared to
slender or straight pitchers because the centre of their pitcher
mass is further away from the growing point on the rosette,
which provides structural support.

Sticky trichomes have repeatedly evolved across multiple
plant lineages, and thus it may be simple to envision the de-
velopment and evolution of the sticky trap type from non-
CPs – though Kaplan and Specht (2020) bring the identity
of sundew tentacles as trichomes into question and proposed,
with support from early observations made by Diels (1906),
that the tentacles are homologous with pinna lobes. In con-
trast to sticky traps, the snap trap has only evolved exactly once
(Dionaea + Aldrovanda clade), and has evoked a more complex
hypothesis for its stepwise evolution from non-CP leaf to sticky
trap to snap trap (Gibson and Waller, 2009). Likewise, one
might imagine pitchers to be developmentally complex. In con-
trast to the expectation that drastic genetic changes would be
needed for transforming a flat leaf into a pitcher, studies on the
development of pitcher leaves in *Sarracenia* (Fukushima et al.,
2015) and the formation of follicle-shaped traps in the carniv-
orous bladderwort genus *Utricularia* (Whitewoods et al., 2020)
indicate that a pitcher-shaped leaf may have evolved through
relatively simple genetic alterations. These genetic alterations
specifically modify the adaxial-abaxial patterning during early
leaf development. In the case of *Sarracenia*, this modification
in tissue patterning is achieved through a distinct pattern of cell
division (Fukushima et al., 2015). While the formation of a
pitcher shape is a crucial step, the existence of a fluid-holding
pitcher structure alone is insufficient for successful nutrient

capture. Instead, the trap leaves must also invest in materials
for prey attraction, retention, digestion and nutrient absorption.
This involves a suite of complex morphological traits including
localized hypertrophy leading to the development of remark-
ably variable and often specialized peristomes and opercula
(Arber, 1941). Thus, physical limits to vascular packing and re-
source provisioning during pitcher development may constrain
the size and complexity of the leaves. Nevertheless, the realiza-
tion that modifying the basic leaf structure is less complicated
than previously assumed offers new perspectives. It suggests
that the primary challenges in the evolution of pitcher leaves
probably lie in areas other than simply altering the overall
leaf shape, and hence there is a need for further study on the
bioenergetics of pitcher leaf development, which arises from
tradeoffs in nutrient and energy capture.

FUNCTIONAL CONSTRAINTS ON PHOTOSYNTHESIS

Most CP leaves, and all pitcher traps, must solve the balancing
act of photosynthetic functioning and nutrient acquisition. As
shown by the cost/benefit model of carnivory, the photosynthetic
costs of carnivorous leaves may not pay off if the environment
is also limited in water and light (Givnish et al., 1984). Pitcher
traps, like other CP leaves, have greatly diminished photosyn-
thetic rates and nutrient use efficiency (PNUE) compared to
typical plants (Ellison, 2006); trap photosynthetic efficiency in-
creases when they are fed (Pavlovič et al., 2009; Pavlovič and
Saganová, 2015). It is currently unclear whether pitchers are
even more inefficient than other types of trap leaves (e.g. sticky
traps), given limited sampling, but there are reasons to suspect
they could be on the lower end of the range within the generally
low photosynthetic rates for unfed CPs. Considering the role
of specific leaf traits, photosynthesis is hypothetically most ef-
fective when a leaf is oriented horizontally, i.e. perpendicular
to the sun; however, for prey retention in a pitfall trap, vertical
trap walls are most effective. In a sufficiently warm, bright and
humid environment, the rate of photosynthesis is directly pro-
portional to the chlorophyll content of a leaf. In other words,
greener leaves may be more efficient at photosynthesizing. On
the other hand, greenness may or may not be an advantage to
pitcher traps as contrasting colours such as red and yellow are
hypothesized to function as attractive signals, as in flowers
(Juniper et al., 1989); however, evidence for the functional
role of red pigments in carnivorous trap leaves is equivocal
(Schaefer and Ruxton, 2008; Bennett and Ellison, 2009; Foot
et al., 2014; Millett et al., 2017; Annis et al., 2018; Gilbert et
al., 2018; Martin-Eberhardt et al. 2025). Pigmentation may,
for example, rather be necessary for photoprotection in open,
sunny habitats. Red pigmentation may correlate strongly with
abiotic (light) gradients at a global scale for sundews (Millett
et al., 2017), while this may or may not be the case for any of
the multiple lineages of pitcher plants. Regardless, pitcher traps
are apparently not constrained by a need for photosynthetic pig-
ments. This is most strikingly apparent in species with white or
translucent patches on their pitchers. This reduced investment
in chlorophyll relative to other pigments (or lack thereof) may
explain why pitcher leaves tend to have especially low photo-
synthetic rates for their LMA, relative to other plants, perhaps
implying that the additional demands on leaves (necessitating
a particular LMA) constrains photosynthetic rates ($A_{max}$) (Farnsworth and Ellison, 2008). Thus, the demands of photosynthetic and carnivorous functions may not necessarily be aligned, which in turn might be the reason for pitcher plants residing on the margins of many leaf trait scaling relationships such as the negative association between $A_{max}$ and LMA.

Relatively few studies have measured a suite of traits of fundamental interest to photosynthetic capacity, such as stomatal traits and leaf thickness (Paluvi and Mukarlina, 2015; Mansur, 2017; Osunkoya and Muntassir, 2017; Meriko and Abizar, 2017; Ghazalli et al., 2019; Huda et al., 2022). Paluvi and Mukarlina (2015) observed intraspecific changes in *Nepenthes* leaf anatomy with light environment consistent with general expectation, namely *N. gracilis* had thinner epidermal leaf thickness in shade compared to open habitat. Of note, the results of this anatomical study were not just limited to the leafy lamina, but held true for the tendrils as well. In addition to leaf thickness, stomatal density also differed, with lower stomatal counts for shade plants. Meriko and Abizar, (2017) looked more specifically at stomatal trait differences across three *Nepenthes* species, *N. gracilis*, *N. reinwardtiana* and *N. ampullaria*. While *N. ampullaria* was classified as being of the anomocytic type, the other two species were classed as the less common actinocytic type with radially arranged subsidiary cells. *Nepenthes reinwardtiana* stood out among the other two species in having a lower stomatal density (~115 per mm² compared to 344 and 323 per mm² in *N. ampullaria* and *N. gracilis*, respectively) and larger stomatal size (11 776 µm² vs. 7360 and 8555 µm² in *N. ampullaria* and *N. gracilis*, respectively). It would be fruitful to combine anatomical studies with physiological data to better understand interspecific variation in photosynthetic efficiency. For instance, Mansur (2017) investigated CO₂ absorption rates in 15 *Nepenthes* species and hybrids. *Nepenthes reinwardtiana* and *N. gracilis* were among these as having amongst the highest CO₂ absorption rates (9.30 and 9.71 µmol m⁻² s⁻¹, respectively); *N. ampullaria* was observed to have the lowest rate (3.74 µmol m⁻² s⁻¹). As it stands, anatomical data are too sparse to draw conclusions on whether stomatal type, size, density or other traits impact CO₂ absorption potential. Mesophyll conductance was found to be an important constraint to photosynthetic efficiency in *Nepenthes* (Capó-Bauçà et al., 2020), and thus more research on leaf anatomy should prove fruitful to this end.

The three major lineages of pitcher plants (Cephalotaceae, Nepenthaceae and Sarraceniaceae) mitigate photosynthetic functional tradeoffs differently (Fig. 1). Species in the Sarraceniaceae rely on a high degree of phenotypic plasticity in pitcher morphology throughout growth and development to separate these two functions temporally. *Darlingtonia* and *Heliamphora* produce juvenile pitchers upon germination that are morphologically distinct (i.e. in pitcher size and shape) from those in adult form. These two leaf forms may show divergent tradeoff strategies between photosynthetic cost and prey capture during development. In *Sarracenia*, certain environmental conditions favour the conversion of the entire leaf into a flat keel, a structure known as a 'phyllodium'. Many species produce phyllodia in late summer when conditions become less favourable for carnivory (Schnell, 1980; Beaulac et al., 2002; Ellison and Gotelli, 2002) or generally in response

to excess nitrogen deposition in the environment, which obviates the benefit of prey capture (Ellison and Gotelli, 2002). Similarly, the pitchers of *Heliamphora* growing in light-limited conditions produce pitchers with reduced carnivorous traits (i.e. elongated pitcher bodies, reduced funnel volume, loss of pigmentation, and nectar production on the pitcher and nectar spoon) as a temporal tradeoff for photosynthesis (McPherson et al., 2011). Likewise, the ratio of anthocyanin to chlorophyll in the forked ‘tongue’ appendage in *Darlingtonia* decreases with sun exposure, indicating that leaves of this species can plasticly respond to light availability with no apparent consequences for prey capture success (Armitage, 2016a). For all these examples, a case can be made for considering the photosynthetic and the trapping leaf phases/parts separately when considering their place in the LES. This is corroborated by the fact that both can have vastly different life spans. Because leaf senescence in pitcher leaves generally begins at the distal end of a leaf, in *Nepenthes*, this results in the photosynthetic lamina outliving its associated trap by months (or possibly years if the period of time prior to trap production is factored in). In Sarraceniaceae leaves, however, the first region to senesce is also the most active region for light capture, but the digestive zone at the shaded base of the leaf can remain alive and function well into a second growing season.

## FUNCTIONAL CONSTRAINTS ON CARNIVORY

While the traditional LES is largely centred on the photosynthetic function of leaves, nutrient acquisition is also a key function of pitcher traps (i.e. carnivory). In this way, the functional analogue for carnivorous pitchers may contain properties of both roots and photosynthetic leaves. Carnivory requires a specific suite of traits, which may have unique sets of costs and tradeoffs distinct from those associated with photosynthesis. Pitchers generally have extrafloral nectaries that attract prey with a sugar reward (i.e. a direct cost in carbon paid to carnivory). Some pitcher plants attract prey through the production of volatile organic compounds (VOCs) (Jaffe et al., 1992; Di Giusto et al., 2008; Jürgens et al., 2009; Ho et al., 2016; Hatcher et al., 2020; Dupont et al., 2023), nectar (Merbach et al., 2001; Bennett and Ellison, 2009) and/or possibly through reflectance patterns (Joel et al., 1985; Moran et al., 1999; Moran et al., 2012), which may all have costs in terms of secondary metabolism. Constraints may be considered in concert or separately across any of the individual functional components of carnivory (attraction, capture, retention, digestion and assimilation of prey nutrients).

While some data support the hypothesized attractive functions of the traits listed above, more experimental work is generally needed to confirm the role of specific traits as signals to specific prey. In contrast to the other four functional components, elucidating animal behaviour is just as critical to empirically probing attractive function as is knowledge from the perspective of the plant. Capture and retention may also involve some elements of animal behaviour, but digestion and assimilation can be broadly understood from plant physiology alone. One complex trapping strategy with strong empirical support from a behavioural experiment is the ‘light-trapping’ strategy found in *Nepenthes aristolochioides*. This species produces
pitchers with a dome-shaped roof and a near-vertically oriented (lateral) opening; the roof has extensive white/translucent patterns ('windows' or 'fenestrations'). Moran et al. (2012) demonstrated that flies (*Drosophila melanogaster*) are attracted to the bright entrance, become disoriented by the false exit of light shining through the back and therefore become trapped. Various pitcher plant species across multiple genera possess such fenestrations, including *Nepenthes klossii*, *Sarracenia minor*, *S. psittacina* and *Darlingtonia californica*. More work is needed to confirm the light-trapping strategy in these other species [but see Schaefer and Ruxton (2014) for *S. minor*]; further, the effectiveness of this strategy on a broader range of insect species remains to be tested.

In contrast to attraction, traits involved in capture and retention are generally better understood on a fundamental, mechanistic level. Most *Nepenthes* possess a collar-shaped pitcher rim (peristome) that turns slippery when wet to capture insects via aquaplaning (Bohn and Federle, 2004; Bauer et al., 2008; Bonhomme et al., 2011b; Lessware et al., 2025). Approximately two-thirds of *Nepenthes* species additionally produce a wax crystal coating on the inner pitcher wall that prevents insect attachment and favours both insects falling into the trap (Juniper et al., 1989; Gaume et al., 2002) and retention of captured prey (Juniper et al., 1989; Gaume et al., 2002, 2004; Di Giusto et al., 2009; Bauer et al., 2012a). The relative length of the waxy zone varies from species to species (Di Giusto et al., 2009; Benz et al., 2012), and a negative correlation has been found between the relative length of the waxy zone and the relative width of the peristome (Benz et al., 2012), suggesting an investment tradeoff for the plants between these two types of slippery structure. Two *Nepenthes* species (*N. gracilis* and *N. pervillei*) are known to produce two distinct forms of wax plates on the pitcher wall and underside of the lid, which function differently, as part of a complex trapping strategy (Bauer et al., 2012b; Chomicki et al., 2024). In this case, ants are able to crawl on the lid underside and only become dislodged when the lid is struck by raindrops in this 'spring-board' trapping strategy; this involves a particular wax platelet morphology and biomechanical modifications to the lid. Interestingly, the springing action of some lids is not a consequence of the springing lids being made of a different material than non-springing lids, but rather relies on *how* that tissue material is arranged (Chomicki et al., 2024). Sarraceniaceae generally have a less prominent waxy layer, but have downward-pointing slippery trichomes (Bauer et al., 2013); however, a few species such as *S. leucophylla*, *S. alata*, *S. flava* and *S. rubra* do have notable wax crystals as well (Poppinga et al., 2010). Pitcher fluid may also be involved in prey capture and retention, as prey drown in the fluid and can be harmed directly by the acidic conditions (Bazile et al., 2015). Pitcher fluid is largely plant-produced (especially in *Nepenthes*), and thus fluid production could hypothetically incur a cost when water is limiting. Pitcher plants, like other CPs, are presumed to be solely adapted to conditions that are not water-limited (Givnish et al., 1984), but some *Nepenthes* species indeed occur in seasonally dry areas (McPherson et al., 2009), so it may be interesting to investigate whether fluid production traits (i.e. volume produced) may vary in these. Some pitcher plant species produce little of their own fluid and instead rely largely on filling up with rainwater;

this includes *Sarracenia purpurea*, *Nepenthes ampullaria* and many *Heliamphora* spp. These species appear to invest less in fluid production, but do not occur in dry environments. Little is known regarding fluid production as a trait, and the selective forces thereof. Several *Nepenthes* produce a sticky, viscoelastic fluid, which has a benefit in increasing prey retention (Gaume and Forterre, 2007; Bonhomme et al., 2011b; Bazile et al., 2015; Kang et al., 2021), and is even more effective on flies than on ants (Bazile et al., 2015). Even watery fluid can have a retention function due to surface tension-lowering compounds that can be plant- or microbially produced, as observed in Sarraceniaceae (Juniper et al., 1989; Armitage, 2016b). Plant-produced viscoelastic fluid composed of polysaccharides may have relatively high metabolic costs similarly to waxes made of long-chain polycarbonates. This is supported by the strong negative correlation observed in *Nepenthes* species between wax density and fluid viscoelasticity (Bonhomme et al., 2011b). Again, this suggests the existence of a tradeoff in the investment of one pitcher trait involved in prey retention over another, the outcome of which may be related to sunlight levels, and/or temperature and humidity, and/or the type of insects predominantly present in the environment. Bonhomme et al. (2011b) observed that the species with the most viscoelastic fluids were most often species growing in mountains, where ants are rarer than in lowlands and flies are more abundant in relative proportions.

Many pitcher plants synthesize a complex cocktail of digestive enzymes that are secreted into the fluid (Saganová et al., 2018; Adamec et al., 2021). Evidence suggests that the proteins present in the digestive fluid of some pitcher plants may be species-specific and could correlate with trapped items (Biteau et al., 2013; Rottloff et al., 2016; Saganová et al., 2018). Inducible enzyme production may reduce the metabolic costs relative to constitutive production (Pavlovič and Saganová, 2015). Furthermore, Rottloff et al. (2016) speculated that even though a particular enzyme is present in the secretome of pitcher plants, fluid pH may influence their activity, possibly rendering them inactive. The exact metabolic costs of the compounds secreted by the pitcher are under-explored, but some species appear to 'outsource' their digestive function to mutualistic microbes or animals they interact with (Lam et al., 2017, 2018a, 2019b; Schöner et al., 2017), presumably offsetting those costs. *Nepenthes ampullaria* and *N. bicalcarata*, for example, may save energy (probably in the form of ATP; see An et al., 2001) by not acidifying the fluid environment to the same extent as other species in favour of outsourcing digestion (Moran et al., 2010; Lam et al., 2019a; Lam and Tan, 2020; Freund et al., 2022; Gilbert et al., 2022). Microbes in particular can take over the functions of enzyme production (Sickel et al., 2016; Kocáb et al., 2021) or even provide a short-cut to nutrient acquisition by fixing atmospheric nitrogen (Prankevicius and Cameron, 1991). Microbial outsourcing of digestive functions has also been found in non-pitcher CPs, with the recent discovery of key enzyme-producing fungi in sundews (Sun et al., 2014); N-fixing bacteria are also known from bladderworts (Sirová et al., 2014). Examining the physiological costs involved in the production of pitcher fluid compounds, the active acidification and overall regulation of the fluid environment, as well as the consequent assimilation of nitrogen and other
<figure><img src="image_3.png" /><figcaption>FIG. 1. The convergent pitcher structures and surfaces of: (A) *Nepenthes*, (B) *Sarracenia* and (C) *Cephalotus*. DZ = digestive zone; L = photosynthetic (non-tubular) lamina of *Nepenthes* (left) and *Cephalotus* (right: note the lamina is not attached to the pitcher); CZ = conductive zone; V = vessel; O = operculum; P = peristome (followed by the letter denoting the genus, as above); bottom right boxes show magnification of peristomes; note the primary ribs (black arrow) and secondary ribs (white arrow) present in *Nepenthes* and *Cephalotus* which are absent in *Sarracenia*. Photo credit: C. Thorogood</figcaption></figure>

nutrients would present a fuller picture of the payoffs involved in carnivory investment.

The quantity and identity of prey ('diet' or 'prey spectrum') can also be considered as a trait or rather the consequence of a constellation of pitcher traits, and thus may also vary among and within species. Considering that carnivory is the primary function of pitchers, there are surprisingly few data on prey capture by pitcher plants. Overall, data on prey capture only exist for *Sarracenia*, *Heliamphora*, *Brocchinia* and *Nepenthes*,

with no documented data from *Darlingtonia*, *Cephalotus* or *Catopsis berteroniana* (Fig. 2). For most studies, taxonomic identification is only to the level of order, and collections made in a single day. This misses variation at finer taxonomic resolutions and variation in prey capture over time, and probably skews prey capture data toward less digestible prey (e.g. beetles and ants). The prey spectra among these pitcher plant lineages are broadly similar, comprising mainly ants (Formicidae), but the quantity and taxonomic composition vary considerably
within and between taxonomic groups of pitcher plants (Kato *et al.*, 1993; Moran, 1996; Adam, 1997; Rembold *et al.*, 2010). This prey capture has been demonstrated to contribute 10–80 % of the total nitrogen content of pitchers/plants (Ellison and Gotelli, 2001). For *Sarracenia*, total prey capture has been quantified for 11 species and hybrids at 43 sites in total, and populations at different sites vary in the amount and composition of prey (Fig. 2; Supplementary Data). For example, the number of prey items in *Sarracenia purpurea* pitchers varied by 20 times between six sites in Britain and Ireland, where the species has naturalized (Whatmore *et al.*, 2022). In two neighbouring *Darlingtonia* populations in Plumas Co., California, average prey biomass in pitchers collected at shaded sampling sites was approximately half that of pitchers collected in sunny habitats, and was positively associated with pitcher leaf size in both habitats (Armitage, 2017).

In *Nepenthes*, prey spectra can differ amongst sympatric species (Chin *et al.*, 2014; Gaume *et al.*, 2016). A reasonable hypothesis is that divergence in the genus may be driven by nutrient competition (Pavlovič, 2012; Thorogood *et al.*, 2018), though direct empirical tests investigating competition are rare (but see Lam *et al.*, 2018b). Several species in Borneo have overlapping distributional ranges and have evolved specializations linked to nutrient sources including particular insect groups (Moran *et al.*, 2001), mammalian faecal capture (Clarke *et al.*, 2009; Greenwood *et al.*, 2011; Schöner *et al.*, 2017) and leaf litter (Moran *et al.*, 2003; Pavlovič *et al.*, 2011). This diversity in pitcher function appears to be the result of an adaptive radiation driven by dietary shifts, analogous to well-known examples in animals, such as the diverse beak shapes of Darwin's finches (Thorogood *et al.*, 2018). However, the trapping mechanisms of most of the ~200 documented species have never been observed. Recent work has used a mathematical modeling approach to provide a theoretical basis for how prey capture may be influenced both by peristome shape and relative size (Moulton *et al.*, 2023). This work suggests prey capture success is linked to geometric complexities, and hints at a fine-tuning of peristome size to optimize capture likelihood for a given shape and size. For example, species such as *N. veitchii* produce a conspicuously broad, oblique peristome. The model predicts that optimal levels of peristome flaring are consistent with those observed in nature, suggesting that these features confer a selective advantage in the capture-versus-construction tradeoff. *Nepenthes veitchii* often forms a distinct tree-climbing habit such that a portion of the peristome touches the vertical axis of the supporting tree. A flared peristome may act as a prey shuttle into the pitfall trap. By contrast, the model predicts that for the production of peristome 'teeth' (prominent spine-like, parallel features in, for example, *N. macrophylla*, *N. diabolica*, *N. villosa* and *N. hamata*), the cost significantly outweighs the benefit. Therefore, these structures – which have evolved independently – probably serve an unidentified function, for instance prey retention. This potential function could be determined by considering the prominent 'fangs' of *N. bicalcarata*, which have been shown to contribute to prey capture (Merbach *et al.*, 1999; Bonhomme *et al.*, 2011a; Thornham *et al.*, 2012); other species with flanges terminating in enlarged toothy projections may function similarly. In *N. hamata*, the highly ordered aquaplaning-promoting microtopography may be restricted to

the flanges and teeth, with less ordered microtopography in flatter areas (U. Bauer, pers. obs.).

Despite some empirical data on the relationship between pitcher morphology and prey spectra in the genus *Nepenthes*, a similar level of detail is lacking for the other pitcher plant taxa, which also display a striking range of variation in pitcher morphology and physiology. For instance, in *Sarracenia*, the size and position of the lid varies from being reflexed away from the pitcher mouth (e.g. *S. purpurea*) to entirely obscuring its entrance (e.g. *S. minor*). Whatmore *et al.* (2022) found that pitchers with wider mouths caught more prey, while Cresswell (1993) also found that larger *Sarracenia purpurea* pitchers caught more prey. Dupont *et al.* (2023) showed that both pitcher size and quantity of VOCs are correlated with quantity and diversity of prey. Together, these studies show there are complex interactions between pitcher form and prey spectrum. Climatic and other environmental conditions as well as the faunal composition in particular habitats may also drive functional constraints. In considering current data on pitcher plant prey spectra, one notable dimension is the degree to which different taxa specialize on ants. At the genus level, *Nepenthes* specialize more on ants on average (~60 % of diet) compared to *Sarracenia* (~40 % of diet comprising ants), and both are dwarfed by *Brochinia* and *Heliamphora* that both have upwards of 90–95 % ant prey (Fig. 2). Within *Nepenthes*, with the exception of the termite-specialist *N. albomarginata*, the species that do not have ants as the majority of their diet tend to be species from higher elevations such as montane *N. kinabaluensis*, *N. lowii*, *N. macrophylla*, *N. muluensis*, *N. sandakanensis*, *N. tentaculata* and *N. villosa* (Fig. 2). Cliff-dwelling *N. campanulata* also has <50 % ant relative abundance. Well-known consequences of elevational gradients on ant abundance could partly explain the general reduction of ants in the diets of high-elevation species (Szewczyk and McCain, 2016). However, more data from understudied pitcher plant lineages are needed to understand the apparent high degree of ant-specialization in the tepui-dwelling *Heliamphora* and *Brochinia* species.

## BUDGETARY CONSTRAINTS ON PHOTOSYNTHETIC FUNCTION

Contrary to the common misconception that CPs are fully heterotrophic, relying solely on nutrients obtained from animal prey, all CPs conduct photosynthesis as their primary source of energy and carbon. In fact, CPs allocate a significant portion of the resources derived from photosynthesis towards trap construction and associated carnivorous functions, such as extrafloral nectar production and digestive enzyme secretion, generating a return on investment from carnivory. In pitcher plants, the photosynthetic cost of functional pitchers might be much higher than that of other CPs with simpler traps, such as sticky glandular traps, because of expensive pitcher construction and maintenance costs along with the photosynthetic inefficiency associated with their tubular shape. This suggests that pitcher plants must delicately balance the tradeoff between photosynthesis and carnivory. Few studies have directly compared the nutrient stoichiometry of carnivorous and
<figure><img src="image_4.png" /><figcaption>FIG. 2. Relative prey abundance of *Nepenthes*, *Brocchinia*†, *Heliamphora* and *Sarracenia* at the species and genus level. *Prey capture includes unquantified vegetation. †*Brocchinia reducta* was the sole species of its genus included in the analysis and therefore was not included in the cross-species comparison.</figcaption></figure>
non-carnivorous plants; Givnish and Shiba (2022) go further
by examining these balances in tissues of both groups of plants
co-occurring in the same bog. Pitchers (Sarracenia) and sun-
dews (Drosera) were similarly nitrogen-limited, but the nu-
trient stoichiometry of aquatic bladderworts (Utricularia) was
distinctly different. Overall, CPs had lower leaf C and N:P
ratios and higher δ¹⁵N (partly due to prey capture) than non-
CPs. More studies like this are needed to definitively parse the
differences in nutrient and photosynthetic balance between
pitchers and other carnivorous traps, and between CP and
non-CP leaves generally; however, some interesting trends re-
garding pitcher budgetary constraints have already emerged
from prior literature.

In optimal environments (sunny, moist and nutrient-poor) where photosynthesis is not limited, the tradeoff between photosynthesis and carnivory influences the ability of pitcher plants to enhance their overall fitness (i.e. through increased photosynthesis and relative growth rate) by obtaining additional nutrients from prey. However, in conditions or environments where the investment in carnivory outweighs the benefits, pitcher plants typically respond by reducing their allocation towards carnivory (e.g. reduction in trap size or quantity). A meta-analysis by Ellison (2006) indicated that increasing prey capture generally enhances growth for CPs, though this effect may be diminished in fertilized soils. In some instances, the plants might even completely forgo their carnivorous function. This diminishment of carnivorous function can take different forms, e.g. the production of flattened, non-carnivorous pitchers for photosynthesis in *Sarracenia* (Ellison and Gotelli, 2002; Ellison et al., 2004) or complete pitcher abortion as observed in *Nepenthes* (Bazile et al., 2012). Further illustrating the interaction between nutrition and trap function, Pavlovič et al. (2009) demonstrated that supplemental feeding in an experimental context increased both net assimilation (A<sub>N</sub>) and pitcher size in *Nepenthes talangensis*. Hence, the tradeoff between photosynthesis and carnivory presents constraints which shape the evolution and ecology of pitcher plants.

In a manipulative field experiment on *Sarracenia alata*, Segala and Horner (2023) tested the combined effects of light availability and prey capture on pitcher morphology, including leaf mass and pitcher aperture diameter, with greater diameters being important for effective prey capture (Heard, 1998; Bhattarai and Horner, 2009). Shading led to a reduction in pitcher diameter, revealing that not only do unusually high nutrient levels (N) tip the payoff balance away from carnivory and towards photosynthesis, but reduced energy from light (C) can also do the same. Segala and Horner (2023) also found that the prevention of prey capture led to a trend of reduced pitcher height. Further, the interaction between shading and feeding treatments was significant; shading significantly reduced leaf mass in fed plants, while shading had no effect on leaf mass in unfed plants. This shows that a lack of nutrient availability may diminish the ability of the plants to respond to changes in light availability.

BUDGETARY CONSTRAINTS ON CARNIVOROUS
FUNCTION

The LES focuses on tradeoffs among traits for the optimal
allocation of nutrients for harvesting of light and CO₂ by a

leaf, and these tradeoffs would be expected to apply to pitcher
plants. Because they are also nutrient-harvesting organs, the
principles of the root economics spectrum may also play a
role: that there is a tradeoff between nutrient exploration and
resource conservation. Understanding how the strategies for
managing the tradeoff between photosynthesis and prey cap-
ture are played out in different ecological situations provides
useful insights into pitcher plant evolution and ecology. These
may also constrain the reproductive ecology of pitcher plants,
potentially limiting the suite of strategies that would be suc-
cessful. Very little is known in this area; nevertheless, traps
often seem to fall somewhere on the LES between low invest-
ment/short life span and high investment/durable. Construction
costs seem to play a role, but there is not just one economically
viable solution. Larger traps tend to be more sturdy, long-lived
and costly (i.e. reinforced with lignin). This might be due to
the demand to be able to withstand higher forces, both from
fluid mass inside the trap, higher wind drag and also poten-
tially larger prey. Lignin and other structural polysaccharides
may in fact not be costly to CPs that grow in wet sunny habi-
tats and are limited by N and P, not by photosynthesis. Several
studies have examined concentrations of nutrients including N,
P, K and trace elements in the tissues of both pitchers and lam-
inae in several species of *Nepenthes* (Osunkoya *et al.*, 2007,
2008; Brearley and Mansur, 2012; Van der Ent *et al.*, 2015;
Brearley, 2021; Mansur *et al.*, 2021, 2022, 2024); such data
can provide pivotal insight into understanding these budgetary
considerations to pitcher functions when combined with data
on prey capture. The potential outsourcing of digestive func-
tions to animal and/or microbial symbionts should also be
considered, as interactions that further modify the outcome of
budgetary balancing.

ENVIRONMENTAL CONSTRAINTS ON CARNIVORY
TRAITS

A clade-wide study of *Nepenthes* (94 species included) by
Moran *et al.* (2013) used ecological niche models to identify
the relationship between bioclimatic covariates such as annual
mean, minimum and maximum temperatures and precipita-
tion with particular classes of pitcher traits (peristome size,
wax presence/absence, viscoelastic fluid). They found that hu-
midity and seasonality were strong predictors of trapping traits
such that pitchers could be classified based on morphology
as belonging to ‘wet’ or ‘dry’ syndromes, with those species
bearing highly specialized pitchers being most associated with
perhumid climates of equatorial Southeast Asia, possibly due
either to increased selection against novel, ‘riskier’ traits at the
clade’s distribution margins, or through increased hybridiza-
tion among *Nepenthes* species in the more species-rich Malay
Archipelago. In a phylogenetic comparative analysis across the
genus (85 species included), *Gilbert et al.* (2018) also found
that species with higher elevational distributions (‘highland’
species) tended to produce shorter laminae and shorter pitchers
(both upper and lower), and had larger peristome ribs com-
pared with lowland species, though there are many exceptions
to these trends. In concert, these results suggest that interspe-
cific differences in trapping traits may be partially attributable
to climatic drivers but further experimental work is needed to
separate population genetic and ecological contributions to
intraspecific pitcher trait plasticity.

Another important study by Gaume et al. (2016) examined interspecific differences in the pitcher traits of six sympatric *Nepenthes* species and how these differences relate to prey capture. They found compelling evidence for prey partitioning in this system such that each species in the community had a pitcher phenotype specialized on a different subset of the local insect community. While it is tempting to attribute these differences to ecological character displacement driven by resource competition, without data on the strength of resource competition among pitcher plants with similar traits, the ecological and evolutionary processes structuring these patterns remain vague. Another important outcome of their study was to demonstrate the extent of intraspecific variation in morphological characters of the seven focal Bornean species. Here, much more variation was observed in *N. bicalcarata* and *N. rafflesiana* pitchers than in *N. ampullaria*, *N. albomarginata*, *N. hemsleyana* or *N. gracilis*. However, the extent of intraspecific pitcher variation (both within and among lower and upper pitchers) was not clearly associated with a broader spectrum of captured prey. Instead, they found more variation at the interspecific level; specifically, prey diversity was positively correlated with pitcher mouth diameter, production of sweet odour and fluid acidity, with *N. rafflesiana* var. *typica* and *N. r.* var. *gigantea* being the most generalist species.

In a Singapore field study of *N. gracilis*, which exhibits polymorphism in pitcher colour, Gilbert et al. (2018) found a strong negative relationship between canopy cover and red pigmentation. This correlation between pigmentation and light environment was also suggested to be relevant more to interactions with herbivores rather than prey or for photoprotection.

To our knowledge, no studies have conducted similar trait-
environment analyses on wild populations of *Heliamphora* or
*Cephalotus*. However, both genera can be found growing across
marked environmental gradients. In the case of *Heliamphora*,
species can be found at the base and tops of tepui mountains
where climatic conditions are considerably different. Likewise,
*Cephalotus follicularis* can be found growing in habitats from
directly adjacent to the ocean to more inland habitats; these
may differ in soil mineral characteristics and osmotic condi-
tions. How these species' traits respond to such gradients re-
mains an open question.

It may be worth mentioning as well that the organisms
that pitcher plant species interact with may also respond
to environmental gradients, thus indirectly influencing
pitcher traits. For instance, ants, a key prey resource, are
known to diminish in abundance with increasing eleva-
tion (Szewczyk and McCain, 2016); also, eukaryotic mi-
crobes living in pitcher fluid were found to be responsive
to elevational gradients as well, though bacteria appear to
be less sensitive to the same external gradient (Gilbert et
al., 2020). In general, to understand environmental con-
straints on carnivory traits across pitcher plant taxa, a
closer look at environmental gradients will be insightful
for finding correlates of variation in pitcher traits –
incorporating morphology, physiology, prey spectra and
symbiont interactions.

ENVIRONMENTAL CONSTRAINTS ON SPATIAL
DISTRIBUTION

Plants' phenotypic traits are shaped in part by their local en-
vironments. That is, it may be more advantageous to possess
certain traits at one end of an ecological gradient than the other,
and this can manifest as either intra- or interspecific trait vari-
ation. Such ecological gradients are ubiquitous in nature and
span scales ranging from centimetres to thousands of kilo-
metres. Pitcher plants growing over such gradients are chal-
lenged to balance the budgetary constraints imposed in the
previous section alongside the additional constraints of specific
ecological pressures arising from both the abiotic and biotic
components of the local environment. Such phenotype–envir-
onment correlations have been documented both within and
among species across the vascular plant phylogeny (Bruelheide
et al., 2018), yet information specific to pitcher plants' mor-
phological tradeoffs and variation over ecological gradients
remains scarce. Most pitcher plant species are relegated to ex-
tremely small geographical ranges, and within these minute
ranges, local populations tend to be further fragmented into
infrequent patches of favourable habitat. Therefore, a reason-
able a priori hypothesis might be that pitcher plants – owing to
the constraints detailed in the previous sections – are prevented
from expressing the levels of phenotypic plasticity or capacity
for adaptive trait divergence that allow them to tolerate even
moderate levels of environmental variation. If so, this has im-
portant consequences for pitcher plant species' range dynamics
and vulnerability to a non-stationary climate.

In this section, we will attempt to understand the determin-
ant s of pitcher plants’ local and regional distributions from the
perspective of their morphological traits. To do so, we will first
review the literature on phenotype–environment correlations in
pitcher plants. We will then contrast pitcher plant taxa in terms
of habitat breadth and geographical range size with the goal of
identifying potential axes of phenotypic variation and tradeoffs
giving rise to these distributional trends.

The North American pitcher plant *Sarracenia purpurea*
shows marked phenotypic variation across its large geograph-
ical range (Schnell, 1979), and is probably the most well-
studied pitcher plant species from the perspective of ecological
trait variation. Factors implicated in pitcher leaf trait variation
(primarily in size and colour) include geographical location
(Whatmore et al., 2022), light availability (Yoon et al., 2019),
prey/nutrient availability (Farnsworth and Ellison, 2008; Yoon
et al., 2019), nitrogen deposition (Ellison and Gotelli, 2002),
substrate pH (Karberg and Gale, 2013), wetland habitat type
(Bott et al., 2008) and regional climate (Freedman et al.,
2021). To date, only one study has combined multiple envir-
onmental factors to determine the most relevant environmental
axes driving phenotypic variation in the species (Ellison et al.,
2004). Here, the authors measured six morphological traits on
*S. purpurea/S. rosea* pitcher leaves from 39 locations spanning
the entire native range of this species complex, and regressed
these traits against principal axes representing aggregated cli-
matic or pore-water chemical variables. The authors detected
weakly significant positive relationships between precipitation
and pitcher size, shape and peristome thickness. Pitchers from
warmer sites tended to be taller and thinner than those from
colder, more northern sites, and pitcher keel size was marginally
positively correlated with increased dissolved nutrients in pore water. Overall, the relationships between morphology and site characteristics – including climate – were relatively weak and much variation in pitcher morphology among sites remained unexplained. One further study assessed latitudinal variation in germination characteristics of *S. purpurea* which, while not directly related to prey trapping adaptations, showed no clear association with latitude (Ellison and Gotelli, 2001).

Studies on spatial variation in pitcher morphology have also been carried out in other Sarraceniaceae. Comparing the morphology of *Sarracenia alata* growing at three neighbouring sites in Louisiana, Green (2006) found significant differences in pitcher height, hood area and funnel diameter between populations growing in a depression bog and a hillside seepage bog. These differences were associated with increased prey biomass by the larger hillside pitchers. In *Darlingtonia californica*, pitcher size peaks occurred at intermediate elevations, with the smallest pitchers at the lowest and highest elevation sites (Ellison and Farnsworth, 2005). While this comparison was only conducted on five populations ranging from 411 to 1241 m above sea level, anecdotal evidence from further *D. californica* populations ranging from sea level to 2000 m elevation generally accord with this trend (D. Armitage, pers. obs.). At high elevations, the small sizes of pitchers are probably due in part to exposed, windy environments and a short growing season. At sea level, while *D. californica* pitchers tend to be smaller, on average, than those at mid-elevations, there are also exceptions, possibly related to habitat quality, which is more variable among low-elevation populations. These size differences may also be genetic rather than environmental, given that one introduced population of *D. californica* in a sub-optimal coastal habitat in Mendocino Co., California, maintained the large stature of its source population from the Northern Sierra Nevada mountains.

Also, seed dispersal limitations may impose range restrictions on pitcher plants and prevent efficient habitat tracking. Seeds of *Sarracenia*, for example, travel an average of <10 cm (Ellison *et al.*, 2012), and while the hydrophobic seeds of Sarraceniaceae might have historically afforded them greater distance, the aquatic conditions required for such extension are more fragmented now than during their pre-Eocene heyday (Ellison, 2001). *Nepenthes* is dioecious, so colonization of both male and female seeds must establish in relatively close proximity in order for new populations to form (Baker, 1955). Germination data for *Cephalotus* suggest that recruitment occurs within a narrow range of environmental conditions (Just *et al.*, 2019), indicating that the window of opportunity is short and restricted. However, like many other functional traits, data on seed traits and dispersal in pitcher plants are relatively sparse in the literature.

## RELATIONSHIP BETWEEN ELEVATIONAL AND GEOGRAPHICAL RANGE IN NEPENTHES

Geographical ranges themselves (and the climate conditions they encompass) can also be considered traits of a species. Species in the Sarraceniaceae and Nepenthaceae tend to occupy small geographical ranges. Within each family, however, there are a small number of 'outlier' species with range sizes

that are at least one order of magnitude larger than is typical for the family, for example *Sarracenia purpurea* in North America and *Nepenthes mirabilis* in Southeast Asia. These outliers may be well adapted to broader environmental conditions; however, this remains unexplored. Another possibility is that some species may have evolved in a time when their preferred niche was less fragmented such as the more ancestral lowland species *Nepenthes mirabilis* and *Nepenthes gracilis*. Many of the small-ranged *Nepenthes* species are endemic to one or a few isolated mountains, and although they sometimes occur there over relatively wide elevational gradients encompassing a range of climate zones, they do not occupy the lowland area that spans the space between mountain ranges. Some *Heliamphora* and many *Nepenthes* species only grow over exceedingly narrow climatic ranges. Highland species thus have greatly constrained niche space and may face greater loss of suitable habitat in the face of climate change (Schwallier *et al.*, 2016; Gray *et al.*, 2017).

While interspecific trait variation is one of the most apparent properties of pitcher plants, and evidence suggests that these traits at least partially covary with climate or other environmental factors, we can begin to assess whether traits of certain large-ranged 'outlier' species discussed above relate to their unique range sizes or environmental tolerances. Taking *Nepenthes* as an example, we can quantify the elevational range of each species as the difference between their highest and lowest observed distributions in the field (Moran *et al.*, 2013). Species with larger elevational ranges could generally be considered to be more tolerant of climate variation than those with very narrow elevational ranges. Since environmental tolerance is also a key determinant of geographical ranges (particularly over latitude), we can also rank *Nepenthes* species by their geographical range sizes, which might also positively covary with environmental breadth. To do so, we first pulled all georeferenced occurrence records of *Nepenthes* from various natural history databases (GBIF), and used them to fit species distribution models (SDMs) which correlate species presences with local climate variables and output a map of habitat suitability (Phillips *et al.*, 2006). By constraining these suitability maps to convex polygons of each species' observed distribution, we can then estimate the overall geographical range sizes of each species (Kass *et al.*, 2022). While this is not a perfect way to estimate the range sizes of species with such limited numbers of occurrence records, it suffices for this illustrative comparative analysis. We asked whether the observed elevational distributions of *Nepenthes* species were associated with range sizes, with the expectation that taxa with wide elevational ranges should also have wide geographical ranges as well. Those species displaying the highest elevational and geographical ranges are anticipated to be few in number, but potentially possess some unique set of traits that might confer wide environmental tolerances.

We found a significant, positive relationship between elevational and geographical range size (Fig. 3). Here, species such as *N. maxima*, *N. reinwardtiana*, *N. ampullaria*, *N. mirabilis* and *N. tentaculata* can be classified as having both the largest geographical ranges and larger than average elevational extents. What common traits, then, might these species share with one another? While there are no single, obvious similarities distinguishing these species from the rest, all do display remarkably high morphological variability in terms of growth
form, pitcher coloration, pitcher size and peristome/operculum shape. However, these variants are typically relegated to very specific localities, rather than appearing repeatedly in similar environments on different landmasses, indicating they may not represent locally adapted ecotypes but rather arise as an evolutionary consequence of these species' large, fragmented ranges.

Intraspecific trait variation arising from phenotypic plasticity is anticipated to be an advantageous trait for widely distributed species. Since few studies have simultaneously assessed intraspecific trait variation in different pitcher plant taxa (but see Chomicki et al., 2024, who examined trapping-related traits in 40+ species), this prediction is difficult to assess. One study to do so measured the morphological traits of eight sympatric Nepenthes species on Mt Kinabalu and Mt Trusmadi in Sabah (Borneo) which included the small-ranged *N. burbidgeae*, *N. rajah*, *N. macrophylla* and *N. villosa* and larger-ranged *N. lowii*, *N. stenophylla*, *N. reinwardtiana* and *N. tentaculata* (Chin et al., 2010). Re-analysis of the authors' data reveals weakly negative trends between the first principal coordinate of pitcher morphology (including pitcher width, depth, height, volume and orifice depth and explaining 83 % of the variance), and both log geographical range size and elevational breadth (Fig. 3). The two species with the largest geographical/elevational ranges (*N. tentaculata* and *N. reinwardtiana*) in this

study were also those with the smallest pitchers. There were, however, no relationships between range sizes and trait variation, as measured by the coefficient of variation. Further, for all morphological traits measured, interspecific variation was, on average, 2.5 times greater than intraspecific variation. This suggests that pitcher traits may be constrained more strongly by species-specific factors such as genetic background, rather than being free to converge on phenotypic optima in a common environment. Future work may take a macroecological perspective by integrating the frequency distributions of quantitative pitcher and leaf traits in Nepenthes to assess whether sympatric communities are non-random subsets of this distribution and to identify more morphological correlates of elevational and geographical range sizes.

## FUTURE DIRECTIONS: WHERE TO GO FROM HERE?

Similar to other plant organs, pitcher leaves of CPs show a broad trait spectrum (variation), both within and among independent lineages. The key to understanding the general ecological drivers and constraints to pitcher traits is leaf economy, which has been successfully explored and applied to other plant organs before and thus applies to pitchers as well. However, given

<figure><img src="image_5.png" /><figcaption>FIG. 3. (A) Relationship between elevational range and geographical range size for Nepenthes species. Here, elevation limits were obtained from Clarke and Moran (2016) and range limits were estimated by fitting ecological niche models (when $n \ge 5$) or 30-km-buffered convex hulls (when $n < 5$) to georeferenced occurrence data. B and C show the relationship between pitcher morphology and elevational/geographical range for sympatric Nepenthes species in Sabah (data from Chin et al., 2010).</figcaption></figure>
# BOX 3. ASSORTED UNANSWERED QUESTIONS AND FUTURE DIRECTIONS

## DEVELOPMENTAL

The low developmental costs of transforming a flat leaf to a pitcher are understood, but less is known regarding the developmental forces shaping intraspecific variation:

* Nepenthaceae produce dimorphic pitchers – what developmental programming regulates the production of upper versus lower pitchers in *Nepenthes*?

* What controls the geometry of the trap shape, i.e. more cylindrical versus rounder pitcher shapes?

* What controls the angle of the lid and orientation of the pitcher aperture?

* Are there any developmental costs to pitcher fluid formation? The total volume of fluid appears to be under genetic control – consider the stable difference in fluid volume between *Nepenthes rafflesiana* and the closely related *N. hemsleyana*, the latter of which produces a lower volume.

* Are there any developmental constraints/costs to pigment pattern formation, including transparent windows found in *Darlingtonia* and *Sarracenia minor*?

* What constraints are there related to the expression of genes and proteins related to carnivory within pitchers and non-pitcher tissues?

* Phytohormones such as abscisic acid, ethylene and gibberellin are known to regulate leaf phenotypic plasticity in non-carnivorous plants. But do they also participate in the plasticity of carnivorous plants? If so, how might their broad, pleiotropic functions lead to developmental or functional constraints that shape their regulatory capacity?

## FUNCTIONAL

* Research on the functional ecology of pitcher trapping mechanisms have thus far focused on adult pitchers, but many pitcher plants including *Sarracenia*, *Heliamphora* and *Nepenthes* have clear morphological differences in the juvenile pitchers produced by seedlings and earlier ontogenetic life stages of the plant. The size and shape of these juvenile pitchers may be suboptimal considering the functional constraints of the adult-form pitchers. Do juvenile pitchers function for prey capture? How do the plants overcome these potential functional costs?

* To what extent do pitcher traits vary, within and between species? How does this variability impact prey capture characteristics, and do certain traits develop at the expense of others?

* What factors go into the regulation of fluid production?

## BUDGETARY

* How do carnivory-photosynthesis tradeoffs change during ontogeny?

* How does the carbon investment (LMA) of carnivorous pitcher plants compare to non-carnivorous leaves in both range (are most CPPs on the high LMA, high leaf longevity end of the LES) and variability?

## ECOLOGICAL

* What is the ecological niche breadth of particular pitcher traits (e.g. trap size, pigmentation, peristomal structure)?

* What are the environmental cues that regulate pitcher expression in *Nepenthes*? Do these cues vary across environments?

* Given that the trapping tissues of Cephalotaceae and Sarraceniaceae are also their centres of photosynthesis, they must be continuously produced by the plant. In contrast, *Nepenthes* can withhold pitcher production but still meet its carbon demands in suboptimal environments. Do these fundamental differences manifest as increased levels of trait-environment correlations in the trapping structures of the former groups relative to the latter?

* If trait-environment correlations in pitcher morphology (and leaf) morphology are rare (as they appear to be) then what aspect of a species' phenotype permits it to have wider environmental tolerances or geographical distributions than small-range congeners?

* Similarly, does the spatial separation of trapping and photosynthetic tissues (e.g. in *Nepenthes*) permit a wider environmental distribution and more interspecific trap variation?
that very little database trait data exist for pitcher plants, biologists must first focus on collecting trait data in a standardized and premeditated way. More specifically, the community must decide on which traits to collect, and by which methodology. Answers to these related questions, therefore, must engage with the observed or hypothesized tradeoffs either in accordance with, or contradicting, the LES. That is, to best understand developmental, functional, budgetary, or ecological constraints on pitcher leaves, which traits must we focus on collecting and comparing? This task and line of questioning has recently been posed for aquatic CPs as well (Bolpagni et al., 2024).

Beyond the constraints discussed thus far, pitcher plants bring novel considerations, which can greatly expand our understanding of the factors shaping leaf construction writ large, whether carnivorous or not. One important insight is that leaves have multiple functions, not just photosynthesis. In the case of pitcher leaves, many key traits function in carnivory: attracting, trapping and digesting prey, and assimilating prey-derived nutrients. A perhaps underappreciated detail is that while roots are generally considered to be the assimilatory organs of non-CPs, leaves in general do have some capacity to uptake nutrients – even without specially adapted absorptive glands – such as via the stomata (Harrison et al., 2000). The predominance of this absorptive function may exist as a gradient across all plants, with CPs and other specialized plants such as tank bromeliads at one end of the extreme. Incorporating this realization into a generalized economics spectrum model may not only improve our understanding of pitcher traits, but better contextualize variation in leaf traits overall.

Some insights may be more restricted to pitcher plants, such as traits that are most important to the trapping of prey. However, even these findings have broader implications for contemplating an expanded model of leaf trait evolution. Consider the springboard trapping mechanism; this is to our knowledge unique to pitcher plants and serves as an illustrative example of how complex traits (relying on multiple interdependent components for its function) can evolve from existing trait variation (Chomicki et al., 2024). Additionally, springboard trapping raises a novel point, which is that certain traits may not be strictly dependent on material construction; rather, the same tissue arranged in different ways may achieve novel biomechanical properties. Much leaf trait work has framed tradeoffs and constraints in terms of construction costs, as we have also done here. However, leaves are not simply static objects, and mechanical properties may come into play even outside of carnivorous contexts as all leaves must deal with wind, rain and the movements of herbivores. Leaf biomechanics clearly matter in trapping strategies, but plants may also exploit the ways leaves are set in motion for the benefit of photosynthesis, e.g. shedding water to preserve photosynthetic efficiency. Thus, to fully understand global leaf trait variation space, simply measuring morphological and biochemical features in isolation may not suffice; more studies should investigate biomechanical features. All in all, many specific questions remain regarding pitcher traits (Box 3), but a lot of recent progress has been made and future directions have been identified. Ultimately, we believe it is possible to create an integrated model of leaf traits that can compare pitchers alongside ‘typical’ leaves; expanding the LES with these novel

insights promises to greatly advance our knowledge even beyond this singular group of plants.

## SUPPLEMENTARY DATA

Supplementary data are available at *Annals of Botany* online and consist of the following. Combined supplementary data.

### FUNDING

K.J.G. was supported by United States Department of Agriculture National Institutes of Food and Agriculture grant 2019-67012-37587. We acknowledge the following sources for funding: the Sofja Kovalevskaja programme of the Alexander von Humboldt Foundation (to K.F.), and JSPS KAKENHI 23K20050 (to K.F.). This material is based upon work supported by the National Science Foundation under Grant No. DEB 2030871 to T.R. Any opinions, findings, conclusions, and recommendations expressed in this material are those of the authors and do not necessarily reflect the views of the National Science Foundation. T.R. and U.B. both acknowledge support from the Human Frontiers Science Program Early Career Grant RGY0082/2021, and T.R. additionally acknowledges support from the USDA National Institute of Food and Agriculture and Hatch Appropriations under Project #PEN04974 and Accession #7006543. U.B. was additionally supported by Royal Society University Research Fellowship URF\R\221028.

### ACKNOWLEDGEMENTS

We thank editor Gitte Petersen for the invitation to write this review, and two anonymous reviewers for their helpful comments on a previous version of the manuscript. This is KBS Contribution #2410.

### DATA AVAILABILITY

Supplemental data and associated code will be made available on the Michigan State University Github repository (https://gitlab.msu.edu/gilbe334/pitcher-economic-spectrum). For the purpose of open access, the authors have applied a Creative Commons Attribution (CC BY) licence to any Author Accepted Manuscript version arising from this submission.

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