Scale-dependent trends in the investment of leaf domatia
←
→
Page content transcription
If your browser does not render page correctly, please read the page content below
Biological Journal of the Linnean Society, 2022, 135, 235–241. With 2 figures.
Scale-dependent trends in the investment of leaf domatia
MATTHEW BIDDICK*,
Terrestrial Ecology Research Group, Technical University of Munich, Freising D-85354, Germany
Received 27 September 2021; revised 6 November 2021; accepted for publication 8 November 2021
Downloaded from https://academic.oup.com/biolinnean/article/135/2/235/6455006 by guest on 03 March 2022
Theory predicts that plants invest in defences proportional to the value or amount of tissue at risk. Domatia-bearing
plants house predatory arthropods that defend against insect and fungal attack. Though leaf domatia represent a
direct investment in the defence of leaf tissues, it remains unknown whether domatia production scales with amount
of tissue at risk. I investigated how domatia investment scales with leaf size in 20 species of trees and shrubs
from the south-west Pacific. Large-leaved species produced more domatia than smaller leaved species. However,
domatia production did not consistently scale with leaf area among individuals of the same species, illustrating that
trends in domatia investment are scale-dependent. Overall results suggest the processes modulating the allocation
of resources to defence at the interspecific level are distinct from those operating at the intraspecific level.
ADDITIONAL KEYWORDS: Coprosma – ecological scales – plant defence – plant functional traits – New
Zealand.
INTRODUCTION Lind et al., 2013; Huot et al., 2014). Similar patterns
arise when plants prioritize growth over defence in
The ability of sessile plants to defend themselves
the early stages of development due to high levels of
against mobile herbivores is paramount to their
competition. Secondly, plants with multiple defences
survival. A plant’s first level of defence is avoidance,
might disproportionately invest in a specific defence
via methods like mimicry, camouflage or rarity
during a given life stage or in response to a specific
(reviewed in Lev-Yadun, 2021). When avoidance fails,
threat (i.e. ‘defence-defence trade-off ’, Dyer et al.,
plants have evolved a myriad of secondary defences
2001; Bingham & Agrawal, 2010; Rasmann et al.,
against herbivory, including physical deterrents, such
2011). More fundamentally, though, plants are
as thorns, prickles and spines (Brown, 1960; Cooper
thought to invest in defences proportional to the value
& Owen-Smith, 1986; Belovsky et al., 1991; Hanley
or amount of tissue that is at risk (i.e. ‘cost-benefit
et al., 2007); non-structural deterrents, such as the
trade-off ’, reviewed in Stamp, 2003). Defensive traits
production of volatile chemicals (Dicke et al., 1993;
should therefore covary closely with the tissues they
Bennett & Wallsgrove, 1994; Kessler & Baldwin,
defend. However, the scale at which this phenomenon
2001); and compensatory growth (McNaughton, 1983;
occurs remains contentious.
Barton, 2008). However, deploying defences imposes a
Leaf domatia are small chambers produced on
physiological cost that can itself hinder plant fitness
the abaxial surface of leaves, which house predatory
(Strauss & Agrawal, 1999), leading to conjecture that
arthropods that defend plants against insect herbivores
plants invest in defences strategically (McKey, 1974,
and fungal attack (Fig. 1; Sampson & McLean, 1965;
1979; Rhoades, 1979; Coley, 1985; Nakano et al., 2020).
Pemberton & Turner, 1989; O’Dowd & Willson, 1991;
Plants can maximize the efficiency of their
Agrawal & Karban, 1997; Norton et al., 2001; Monks
investment into defences in several ways. Firstly,
et al., 2007). Here, I explore domatia investment in
plants might deploy defences at specific life stages,
19 species endemic to New Zealand and one species
during which plants are most susceptible to attack,
endemic to Lord Howe Island. Because leaf domatia
thereby maximizing resources available for growth
are an investment in the protection of leaf tissue
when herbivore and pathogen risk is comparatively
(O’Connell et al., 2010), I hypothesized that investment
low (i.e. ‘growth-defence trade-off ’, Burns, 2013;
in leaf domatia would scale relative to the amount of
leaf tissue susceptible to attack (i.e., leaf size). More
*E-mail: matt.biddick@tum.de specifically, I predicted that the number of domatia
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2022, 135, 235–241 235
This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://
creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided
the original work is properly cited.236 M. BIDDICK
Downloaded from https://academic.oup.com/biolinnean/article/135/2/235/6455006 by guest on 03 March 2022
Figure 1. Example images of domatia types, including: (a) section through a Carpodetus serratus tuft domatium (credit:
Morgan Ngata); (b) Coprosma macrocarpa large pit domatia; (c) Elaeocarpus dentatus tent domatia; and (d) Coprosma
lanceolaris tent domatia.
per leaf would scale positively with leaf lamina area at exist (e.g., leaf scanners, image recognition software
both the inter- and intraspecific levels. and the ad hoc 2/3 correction factor). I explored
shape-specific correction factors, which provide more
accurate estimates of true leaf lamina area (Schrader
et al., 2021). However, leaf shape did not vary widely in
MATERIALS AND METHODS
the taxa considered, with 19 of the 20 taxa producing
Data collection took place between June 2018 and April leaves that are some form of ellipse or obovate with
2019. To explore the relationship between leaf size and entire margins (correction factors of 0.69 and 0.67,
domatia investment, the number of domatia per leaf, respectively). Further, none of the taxa considered are
in addition to leaf length and width was measured deeply lobed: a morphology that produces the greatest
in 20 species from four geographic locales that span overestimates of leaf area when length × width
10 degrees of latitude of the south-west Pacific (Table 1). calculations are used (see Schrader et al., 2021). Thus,
When possible, for each species, a single leaf from length × width estimates sufficed for the purposes of
each of 30 adult individuals was measured using a this study. Domatia were counted systematically in a
digital calliper. Leaves were measured in situ and basipetal direction with the aid of an USB dissecting
care was taken not to damage the plant. Leaf length microscope. Care was taken to ensure that domatia
was measured as the longest distance from the base with multiple openings were only counted once.
of the petiole to the terminal leaf end. Leaf width was To test whether domatia investment scales with leaf
measured as the widest distance perpendicular to the size at the interspecific level, a linear model regression
leaf length measurement. Lamina area (hereafter ‘leaf of mean number of domatia per leaf against mean
size’) was calculated as leaf length multiplied by leaf leaf size was run. Both variables were logarithm-
width. More accurate methods of estimating leaf area transformed prior to analysis to conform to model
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2022, 135, 235–241TRENDS IN DOMATIA INVESTMENT 237
Table 1. List of 20 species used to investigate the association between domatia production (per leaf) and leaf size (lamina
area, cm2). Samples sizes are denoted in parentheses (leaves and individuals, respectively). Correlation coefficients (r),
T-values and P-values are derived from individual within-species linear model regressions. Dashes denote species that
were excluded from intraspecific-level analysis because domatia were not observed, although the species are reported to
produce them
Species Family Locality No. of Leaf r T P
domatia area
Carpodetus serratus (30, 30) Rousseaceae Otari, Wellington 9.26 12.88 0.814 12.058 < 0.001 ***
Coprosma areolata (30, 7) Rubiaceae Otari, Wellington 1.74 2.60 0.189 2.783 0.009 **
Coprosma ciliata (30, 30) Rubiaceae Nelson Lakes 7.03 0.59 0.019 -0.735 0.469
Downloaded from https://academic.oup.com/biolinnean/article/135/2/235/6455006 by guest on 03 March 2022
Coprosma colensoi (30, 30) Rubiaceae Nelson Lakes 0.20 0.49 0.012 -0.577 0.569
Coprosma depressa (30, 30) Rubiaceae Nelson Lakes 0.53 0.09 0.021 -0.772 0.447
Coprosma fetidins (30, 30) Rubiaceae Nelson Lakes 5.17 0.92 0.306 1.702 0.098
Coprosma grandifolia (30, 30) Rubiaceae Zealandia, 13.45 104.45 0.274 3.401 0.002 **
Wellington
Coprosma lanceolaris (30, 30) Rubiaceae Lord Howe Island 1.62 15.88 0.008 -0.297 0.772
Coprosma linariifolia (30, 30) Rubiaceae Nelson Lakes 5.17 4.27 0.305 1.691 0.102
Coprosma lucida (30, 15) Rubiaceae Otari, Wellington 12.62 56.86 0.129 3.656 0.071
Coprosma macrocarpa (30, 30) Rubiaceae Nelson Lakes 0.27 0.24 0.344 3.813 < 0.001 ***
Coprosma perpusilla (30, 30) Rubiaceae Nelson Lakes 0.00 0.77 — — —
Coprosma propinqua (30, 30) Rubiaceae Zealandia, 1.70 0.31 0.027 -1.347 0.188
Wellington
Coprosma pseudocuneata Rubiaceae Nelson Lakes 0.00 0.49 — — —
(30, 30)
Coprosma repens (30, 30) Rubiaceae Otari, Wellington 6.89 28.62 0.562 3.656 0.001 **
Coprosma rhamnoides (30, 30) Rubiaceae Otari, Wellington 0.93 0.48 0.001 -0.156 0.877
Coprosma robusta (30, 30) Rubiaceae Otari, Wellington 9.86 35.42 0.034 -1.017 0.317
Elaeocarpus dentatus (30, 15) Elaeocarpaceae Otari, Wellington 5.56 23.98 0.109 -2.132 0.042 *
Pennantia corymbosa (30, 10) Pennantiaceae Otari, Wellington 4.33 14.49 0.823 10.399 < 0.001 ***
Vitex lucens (30, 8) Lamiaceae Otari, Wellington 25.25 66.60 0.253 3.188 0.004
***, ** and * denote P < 0.001, P < 0.01 and P < 0.05, respectively.
assumptions. A second analysis, at the interspecific domatia per leaf. Leaf size was also diverse, ranging
level and restricted to the Coprosma genus (16 from 0.09–104.45 cm2 (mean = 18.84, lamina area).
taxa), was run to test whether results are sensitive At the interspecific level, domatia investment was
to differences in phylogeny. To test whether domatia positively correlated with leaf size (d.f. = 19, T = 6.315,
investment scales with leaf size at the intraspecific P < 0.001). Large-leaved species produced more
level, individual within-species linear model domatia per leaf than smaller leaved species (Fig. 2).
regressions of number of domatia per leaf against Results did not change when analysis was restricted
leaf size were run. Variables were left untransformed to the Coprosma genus (d.f. = 15, T = 5.067, P < 0.001).
for all within-species analyses. To assess whether C o n t r a s t i n g l y, d o m a t i a i n v e s t m e n t a t t h e
domatia-leaf size scaling relationships are associated intraspecific level was generally unrelated to leaf
with overall leaf size, a linear model regression of size (Table 1). Most species did not invest in domatia
species slope parameters (derived from intraspecific proportional to the size of leaf. Domatia production
scaling) against mean leaf area was run. All statistical in only seven of the 20 species observed scaled with
analyses were performed in the R environment (R leaf size—one of which (Elaeocarpus dentatus)
Core Team, 2020). unexpectedly exhibited the reverse relationship.
Instead, domatia-leaf scaling was generally stronger
in species with greater mean number domatia per leaf
(Supporting Information, Fig. S1, d.f. = 17, T = 2.188,
RESULTS
P = 0.044), such as Carpodetus serratus (T = 12.058,
Domatia investment varied widely among the 20 P < 0.001), Coprosma areolata (T = 2.783, P = 0.009),
species observed, ranging from 0–25.25 (mean = 5.58) Coprosma grandifolia (T = 3.401, P = 0.002), Coprosma
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2022, 135, 235–241238 M. BIDDICK
plants are thought to deploy defences strategically,
simultaneously maximizing the benefits of defence and
minimizing costs to reproduction and growth (reviewed
in Agrawal, 2007). For instance, Acacia trees grown
in the absence of large herbivores and subsequently
subjected to simulated browsing respond with an
increase in spine length (Young et al., 2003). If large
leaves represent a greater potential loss to growth and
reproduction than small leaves, then large-leaved taxa
may invest more in domatia for the same reasons that
Acacia trees upregulate spine production when subject
Downloaded from https://academic.oup.com/biolinnean/article/135/2/235/6455006 by guest on 03 March 2022
to browsing.
An alternative explanation is that the relationship
between domatia number and leaf size represents
simple allometric scaling, as opposed to a selection for
greater investment in domatia in large-leaved species.
Physiologically linked traits are known to covary at
various levels of analysis (Niklas, 1994; Westoby &
Wright, 2003; Sun et al., 2005; Laughlin et al., 2017;
Figure 2. Among-species relationship between domatia Biddick et al., 2018). Whether the allometric scaling
investment (per leaf, y-axis) and leaf area (in cm2, x-axis) in observed in this study represents a physiological
19 species endemic to New Zealand and one species endemic co-dependency is not yet known. All leaf domatia
Lord Howe Island. Large-leaved species produce more considered in this study are produced at the axis of the
domatia than smaller leaved species. Open circles denote midrib and secondary veins (though domatia can also
species means. Both axes are logarithm transformed. be found at the axes of tertiary veins in some taxa). The
disproportionate abundance of domatia in large-leaved
species, therefore, may arise from the simple fact that,
in the mean, large leaves bear more secondary veins
repens (T = 3.656, P = 0.001), Elaeocarpus dentatus than small leaves. Indeed, architectural constraints
(T = -2.132, P = 0.042) and Pennantia corymbosa have been shown to underly size-related patterns of
(T = 10.399, P < 0.001). defensive traits like extrafloral nectaries (Villamil
et al., 2013). However, the inverse relationship between
domatia number and leaf size seen in Elaeocarpus
dentatus casts doubt on allometry as the sole driver
DISCUSSION
of the observed relationship. Further, domatia number
Domatia investment varied widely across the 20 species was unrelated to leaf size at the intraspecific level in
examined. Large-leaved species generally produced more than half of the taxa considered.
more domatia per leaf than smaller leaved species. Theory predicts that, at the individual plant level,
Domatia investment also varied considerably within defences are allocated to tissues in direct proportion
species. However, no consistent relationship between to the probability that they will be attacked (McKey,
domatia production and leaf size was observed at the 1974, 1979; Rhoades, 1979; Zangerl & Rutledge, 1996).
intraspecific level. Seven species exhibited significant Although larger leaves represent a greater potential loss,
domatia-leaf size scaling at the intraspecific level, within species, domatia investment did not consistently
one of which unexpectedly exhibited a negative scale with leaf size. One possible explanation for
relationship. Results therefore illustrate that trends variation in intraspecific domatia-leaf size scaling is
in domatia investment are scale dependent. Further, domatia investment itself. Heavily defended species,
they suggest that the processes modulating investment by chance alone, have a greater capacity for scaling
in plant defence at the interspecific level are distinct relative to less defended species owing to their greater
from those operating at the intraspecific level. variance in domatia number (i.e., domatia size does
Several factors may explain why large-leaved not scale isometrically with leaf size). Indeed, scaling
species exhibited the greatest investment into domatia relationships were strongest in species with higher
production. Many forms of plant defence are considered domatia investment (Supporting Information, Fig. S1).
costly because they consume resources that could To this end, investment trends in small-leaved species
otherwise be allocated to reproduction or vertical and might be better viewed in a ‘presence-absence’ context.
horizontal growth, which increase individual fitness Differences in domatia investment, particularly
(Hare et al., 2003; Fornoni et al., 2004). Consequently, on a per leaf basis, presumably vary with domatia
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2022, 135, 235–241TRENDS IN DOMATIA INVESTMENT 239
type. Most species observed in this study produce pit REFERENCES
domatia, although both tent and tufted domatia were
Agrawal AA. 2007. Macroevolution of plant defense strategies.
also present. Pit domatia are ubiquitous in the genus
Trends in Ecology & Evolution 22: 103–109.
Coprosma and are therefore likely a basal trait that has
Agrawal AA, Karban R. 1997. Domatia mediate plant-
been maintained throughout the radiation of Coprosma arthropod mutualism. Nature 387: 562–563.
in the south-west Pacific (Cantley et al., 2016). Leaf Albert CH, Grassein F, Schurr FM, Vieilledent G, Violle C.
domatia may therefore be a trait that is generally 2011. When and how should intraspecific variability be
phylogenetically conserved; however, this requires considered in trait-based plant ecology? Perspectives in Plant
further study. Interestingly, Coprosma lanceolaris, a Lord Ecology, Evolution and Systematics 13: 217–225.
Howe Island endemic, has evolved highly conspicuous Barton KE. 2008. Phenotypic plasticity in seedling defense
tent domatia. Tent domatia are typically much larger strategies: compensatory growth and chemical induction.
Downloaded from https://academic.oup.com/biolinnean/article/135/2/235/6455006 by guest on 03 March 2022
than both pit and tufted domatia, enabling them to Oikos 117: 917–925.
support a greater abundance of mutualist arthropods. Barton KE. 2014. Prickles, latex, and tolerance in the endemic
As such, trends in the investment of tent domatia are Hawaiian prickly poppy (Argemone glauca): variation
likely distinct from those other domatia types. between populations, across ontogeny, and in response to
Many ecological relationships are scale dependent abiotic factors. Oecologia 174: 1273–1281.
(Blackburn et al., 2002; Burns & Beaumont, 2009). Barton KE. 2016. Tougher and thornier: general patterns in
Recent work has attempted to unify patterns at the induction of physical defence traits. Functional Ecology
distinct ecological scales to better understand the 30: 181–187.
how they arise mechanistically (see Jung et al., 2010; Belovsky GE, Schmitz OJ, Slade JB, Dawson TJ. 1991.
Albert et al., 2011; Laughlin et al., 2017). Results Effects of spines and thorns on Australian arid zone
from this study reinforce the benefit of studying trait herbivores of different body masses. Oecologia 88: 521–528.
Bennett RN, Wallsgrove RM. 1994. Secondary metabolites
relationships across different scales (cf. Hulshof &
in plant defence mechanisms. New Phytologist 127: 617–633.
Swenson, 2010; Lepš et al., 2011; Kichenin et al., 2013).
Biddick M, Hutton I, Burns KC. 2018. Independent evolution
Future studies should employ multi-scale and multi-
of allometric traits: a test of the allometric constraint
trait approaches to better understand the drivers of
hypothesis in island vines. Biological Journal of the Linnean
scale-dependent trait relationships (cf. Ottaviani & Society 126: 203–211.
Marcantonio, 2021). Bingham RA, Agrawal AA. 2010. Specificity and trade-offs
Caution should of course be taken when drawing in the induced plant defence of common milkweed Asclepias
conclusions about large-scale theories underpinning syriaca to two lepidopteran herbivores. Journal of Ecology
the evolution and ecology of plant defence from patterns 98: 1014–1022.
observed in a small group of species. The present Blackburn TM, Gaston KJ. 2002. Scale in macroecology.
study nevertheless provides early steps towards a Global Ecology and Biogeography 11: 185–189.
more comprehensive understanding of trends in the Brown WL. 1960. Ants, acacias and browsing mammals.
production of leaf domatia in the New Zealand flora. Ecology 41: 587–592.
Future work should investigate similar patterns in Burns KC. 2013. Are there general patterns in plant defence
other genera, in addition to exploring how they might be against megaherbivores? Biological Journal of the Linnean
influenced by biogeographic variables such as latitude, Society 111: 38–48.
altitude and insularity (cf. Bowen & Van Vuren, 1997; Burns KC, Beaumont SAM. 2009. Scale-dependent trait
Barton, 2014, 2016; Meredith et al., 2019; Moreira et al., correlations in a temperate tree community. Austral Ecology
2014, 2021; Moreira & Abdala-Roberts, 2021). 34: 670–677.
Bowen L, Van Vuren D. 1997. Insular endemic plants lack
defenses against herbivores. Conservation Biology 11:
ACKNOWLEDGEMENTS 1249–1254.
Cantley JT, Markey AS, Swenson NG, Keeley SC. 2016.
I am indebted to Prof. KC Burns for his academic Biogeography and evolutionary diversification in one of
mentorship earlier in my career. I am also grateful to Dr. the most widely distributed and species rich genera of the
Gian Ottoviani and two anonymous reviewers for their Pacific. AoB Plants 8: plw043.
comments in improving this manuscript. Finally, thank Coley PD, Bryant JP, Chapin FS. 1985. Resource availability
you to J. Schmack for her ongoing love and support. The and plant antiherbivore defense. Science 230: 895–899.
author has no conflict of interest to declare. Cooper SM, Owen-Smith N. 1986. Effects of plant spinescence
on large mammalian herbivores. Oecologia 68: 446–455.
Dicke M, Van Baarlen P, Wessels R, Dijkman H. 1993.
DATA AVAILABILITY Herbivory induces systemic production of plant volatiles that
All related data are available from the author upon attract predators of the herbivore: extraction of endogenous
request. elicitor. Journal of Chemical Ecology 19: 581–599.
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2022, 135, 235–241240 M. BIDDICK
Dyer LA, Dodson CD, Beihoffer J, Letourneau DK. 2001. McKey D. 1974. Adaptive patterns in alkaloid physiology. The
Trade-offs in antiherbivore defenses in Piper cenocladum: American Naturalist 108: 305–320.
ant mutualists versus plant secondary metabolites. Journal McKey D. 1979. The distribution of secondary compounds
of Chemical Ecology 27: 581–592. within plants. In: Rosenthal GA, Janzen DH,
Fornoni J, Valverde PL, Nunez-Farfan J. 2004. Population Applebaum SW, eds. Herbivores, their interaction with
variation in the cost and benefit of tolerance and resistance secondary plant metabolites. New York: Academic Press,
against herbivory in Datura stramonium. Evolution 58: 55–134.
1696–1704. McNaughton S. 1983. Compensatory plant growth as a
Hanley ME, Lamont BB, Fairbanks MM, Rafferty CM. response to herbivory. Oikos 40: 329–336.
2007. Plant structural traits and their role in anti-herbivore Monks A, O’Connell DM, Lee WG, Bannister JM,
defence. Perspectives in Plant Ecology, Evolution and Dickinson KJ. 2007. Benefits associated with the domatia
Systematics 8: 157–178. mediated tritrophic mutualism in the shrub Coprosma
Downloaded from https://academic.oup.com/biolinnean/article/135/2/235/6455006 by guest on 03 March 2022
Hare JD, Elle E, van Dam NM. 2003. Costs of glandular lucida. Oikos 116: 873–881.
trichomes in Datura wrightii: a three-year study. Evolution Moreira X, Abdala-Roberts L. 2021. A roadmap for future
57: 793–805. research on insularity effects on plant-herbivore interactions.
Harper JL. 1989. The value of a leaf. Oecologia 80: 53–58. Global Ecology and Biogeography. Available at: https://doi.
Hulshof CM, Swenson NG. 2010. Variation in leaf functional org/10.1111/geb.13401
trait values within and across individuals and species: an Moreira X, Castagneyrol B, García-Verdugo C, Abdala-
example from a Costa Rican dry forest. Functional Ecology Roberts L. 2021. A meta-analysis of insularity effects on
24: 217–223. herbivory and plant defences. Journal of Biogeography 48:
Huot B, Yao J, Montgomery BL, He SY. 2014. Growth- 386–393.
defense tradeoffs in plants: a balancing act to optimize Moreira X, Mooney KA, Rasmann S, Petry WK, Carrillo-
fitness. Molecular Plant 7: 1267–1287. Gavilán A, Zas R, Sampedro L. 2014. Trade-offs between
Jung V, Violle C, Mondy C, Hoffmann L, Muller S. constitutive and induced defences drive geographical and
2010. Intraspecific variability and trait-based community climatic clines in pine chemical defences. Ecology Letters 17:
assembly. Journal of Ecology 98: 1134–1140. 537–546.
Kessler A, Baldwin IT. 2001. Defensive function of herbivore- Nakano S, Oguro M, Itagaki T, Sakai S. 2020. Florivory
induced plant volatile emissions in nature. Science 291: defence: are phenolic compounds distributed non-randomly
2141–2144. within perianths? Biological Journal of the Linnean Society
Kichenin E, Wardle DA, Peltzer DA, Morse CW, 131: 12–25.
Freschet GT. 2013. Contrasting effects of plant inter- and Niklas KJ. 1994. Plant allometry: the scaling of form and
intraspecific variation on community-level trait measures process. Chicago, Illinois, USA: University of Chicago Press.
along an environmental gradient. Functional Ecology 27: Norton AP, English-Loeb G, Belden E. 2001. Host plant
1254–1261. manipulation of natural enemies: leaf domatia protect
Laughlin DC, Lusk CH, Bellingham PJ, Burslem DF, beneficial mites from insect predators. Oecologia 126:
Simpson AH, Kramer-Walter KR. 2017. Intraspecific trait 535–542.
variation can weaken interspecific trait correlations when O’Connell DM, Monks A, Lee WG, Downs TM,
assessing the whole-plant economic spectrum. Ecology and Dickinson KJ. 2010. Leaf domatia: carbon-limited indirect
Evolution 7: 8936–8949. defence? Oikos 119: 1591–1600.
Lepš J, de Bello F, Šmilauer P, Doležal J. 2011. Community O’Dowd DJ, Willson MF. 1991. Associations between
trait response to environment: disentangling species mites and leaf domatia. Trends in Ecology & Evolution 6:
turnover vs intraspecific trait variability effects. Ecography 179–182.
34: 856–863. Ottaviani G, Marcantonio M. 2021. Precipitation seasonality
Lev-Yadun S. 2021. Avoiding rather than resisting herbivore promotes acquisitive and variable leaf water-economics traits
attacks is often the first line of plant defence. Biological in southwest Australian granite outcrop species. Biological
Journal of the Linnean Society 134: 775–802. Journal of the Linnean Society 133: 411–417.
Lind EM, Borer E, Seabloom E, Adler P, Bakker JD, Pemberton RW, Turner CE. 1989. Occurrence of predatory
Blumenthal DM, Crawley M, Davies K, Firn J, and fungivorous mites in leaf domatia. American Journal of
Gruner DS, Harpole WS, Hautier Y, Hillebrand H, Botany 76: 105–112.
Knops J, Melbourne B, Mortensen B, Risch RC, Rasmann S, Erwin AC, Halitschke R, Agrawal AA. 2011.
Schuetz M, Stevens C, Wragg PD. 2013. Life-history Direct and indirect root defences of milkweed (Asclepias
constraints in grassland plant species: a growth-defence syriaca): trophic cascades, trade-offs and novel methods for
trade-off is the norm. Ecology Letters 16: 513–521. studying subterranean herbivory. Journal of Ecology 99: 16–25.
Meredith FL, Tindall ML, Hemmings FA, Moles AT. 2019. Rhoades DF. 1979. Evolution of plant chemical defense against
Prickly pairs: the proportion of spinescent species does not herbivores. In: Rosenthal GA, Janzen DH, Applebaum SW,
differ between islands and mainlands. Journal of Plant eds. Herbivores, their interaction with secondary plant
Ecology 12: 941–948. metabolites. New York: Academic Press, 3–54.
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2022, 135, 235–241TRENDS IN DOMATIA INVESTMENT 241
Sampson FB, McLean J. 1965. A note on the occurrence of R Core Team. 2000. R language definition. Vienna: R
domatia on the under side of leaves in New Zealand plants. Foundation for Statistical Computing.
New Zealand Journal of Botany 3: 104–112. Villamil N, Márquez-Guzmán J, Boege K. 2013.
Schrader J, Shi P, Royer DL, Peppe DJ, Gallagher RV, Understanding ontogenetic trajectories of indirect defence:
Li Y, Wang R, Wright IJ. 2021. Leaf size estimation based ecological and anatomical constraints in the production of
on leaf length, width and shape. Annals of Botany 128: extrafloral nectaries. Annals of Botany 112: 701–709.
395–406. Westoby M, Wright IJ. 2003. The leaf size-twig size spectrum
Stamp N. 2003. Out of the quagmire of plant defense and its relationship to other important spectra of variation
hypotheses. The Quarterly Review of Biology 78: 23–55. among species. Oecologia 135: 621–628.
Strauss SY, Agrawal AA. 1999. The ecology and evolution of Young TP, Stanton ML, Christian CE. 2003. Effects of
plant tolerance to herbivory. Trends in Ecology & Evolution natural and simulated herbivory on spine lengths of Acacia
14: 179–185. drepanolobium in Kenya. Oikos 101: 171–179.
Downloaded from https://academic.oup.com/biolinnean/article/135/2/235/6455006 by guest on 03 March 2022
Sun S, Jin D, Shi P. 2005. The leaf size-twig size spectrum of Zangerl AR, Rutledge CE. 1996. The probability of attack
temperate woody species along an altitudinal gradient: an and patterns of constitutive and induced defense: a test
invariant allometric scaling relationship. Annals of Botany of optimal defense theory. The American Naturalist 147:
97: 97–107. 599–608.
SUPPORTING INFORMATION
Additional Supporting Information may be found in the online version of this article at the publisher’s web-site:
Figure S1. Relationship between domatia-leaf size slope and number of domatia per leaf.
© 2021 The Linnean Society of London, Biological Journal of the Linnean Society, 2022, 135, 235–241You can also read
