Fern functional trait differences: the mechanism for fern species coexistence in the
E. A. Lawrence
Abstract – Understanding community assembly is key for an appreciation of how present
ecosystems were established, and how they might change in the future. Habitat5
heterogeneity and species’ functional trait diversity were examined as potential species
coexistence mechanisms for ferns in Catlins’ forest. Differences in environmental traits
between tree-type characterised sites and fern functional trait diversity was analysed in
order to determine the dominant mechanism dictating community composition. Results
suggested that there was little variation between tree-type characterised sites, whereas10
fern species differed significantly in many assessed traits. Hence, functional trait diversity
was favoured as the prevailing coexistence mechanism.
Ecological communities are hugely complex systems, structured with patterns of
abundance and diversity that determine the overall species assemblage (Simberloff,15
2010). The challenge of understanding such systems has long interested plant ecologists,
driving the development of many theories – with evasive consensus (Zobel et al., 1994).
With the aim of simplifying the proposed ideas, these theories regarding community
composition have been distilled into a handful of potential mechanisms.
Two such ideas that are regularly compared are that of niche heterogeneity and spatial20
heterogeneity (Zobel et al., 1994; Brown, 1995; Cornell & Lawton, 1992). In the
approach to the question of community structure, these theories assume differences in
resource use between species – through diverse functional traits and diverse habitat
preferences respectively. To expand on this, through niche heterogeneity species have
diverse functional characteristics and therefore different resource use and requirements,25
minimising competition in homogenous local environments (Brown, 1995).
Alternatively, environmental heterogeneity may have the greater role in community
diversity (Smith & Lundholm, 2012), with different species advantaged in different
habitats within a particular environment, dominating microsites (i.e. very immediate
environment) and thus avoiding direct interspecific competition (Zobel et al., 1994).30
Regardless of science’s attempts to isolate the predominant mechanism, competitive
exclusion is evidently being managed successfully to account for the prevailing species
The mediation of species coexistence ensures the persistence of richly biodiverse
communities, which in turn supports productivity and stability within ecosystems (Beck,35
2013). While the development of an understanding of how particular floral communities
are structured is intrinsically valuable, the knowledge gained through the study of
diversity maintenance mechanisms will also have greater significance in application to
managing changes linked to a changing environment. As is increasingly apparent, the
influence on the natural environment of anthropogenic actions is pronounced, changing40
climate and exposing plant communities to new pressures (IPCC, 2014; Walther, 2010).
Increasing our understanding of how concurrent plant species interact – leading to how
their communities are structured – will enable better preparation in addressing issues that
may arise in the field of biodiversity conservation and maintenance of ecosystem services
(Díaz & Cabido, 2001).45
In the study of community composition, the rainforest is particularly relevant with a
characteristic dense co-occurrence of highly diverse plants. Most notable in the
understory is competition between species subordinate to, and limited by, the canopy
above. With resource access compromised in this environment – trees dominate and alter
site conditions (Ovington, 1955) – the persisting abundance and diversity of understory50
species is interesting.
The temperate rainforests of New Zealand are one such environment where a rich
assembly of species can be observed (Allen et al., 2013). Representing 7.5% of the
country’s indigenous vascular flora, New Zealand’s ferns are an important feature of the
forest ecosystem (Lehmann et al., 2002). Despite their notable presence, relatively few55
publications examine fern ecology. The 173 species present on these islands – with almost
half endemic – display marked diversity in growth forms, offering great scope for study
and furthering this limited field (Lehmann et al., 2002).
Temperate rainforests on the Catlins coast, Otago, offer a diverse assemblage of fern
species, which coexist beneath a native podocarp-hardwood canopy (Tocher et al., 2000).60
Ferns species that occur in this environment are observed to exhibit wide morphological
variation, and the author has observed many co-occurring across a small spatial scale.
The present study aimed to identify the mechanism at work in the Catlins which mediates
fern species coexistence. Following proposals from similar literature, two hypotheses
were focussed on as potential coexistence mechanisms – habitat heterogeneity and65
functional trait diversity (Zobel et al., 1994; Brown, 1995; Cornell & Lawton, 1992).
Our approach simultaneously examined the variation in environmental traits between
forest types and trait variation between the present fern species. Forest type was defined
by the dominant tree type at each sampling site – gymnosperm or angiosperm. Previous
studies report that gymnosperm trees are slow-growing, forming open canopies which70
allow higher understory soil temperatures and light levels (Boggs & McNulty, 2010;
Anderson et al., 1969). Conversely, angiosperm trees create denser canopies, leading to
a shady and humid understory (Watkins & Cardelús, 2012; Friis et al., 1987). Trees have
been suggested to act as ‘ecosystem engineers’, defining the habitat structure, and biotic
and abiotic conditions within an ecosystem (Jones et al., 1994). We might expect to see75
environmental differences between site types based on their differing ‘dominant’ trees.
With this and the coexistence hypotheses in mind, I questioned whether there is
significant habitat heterogeneity between tree-type defined sites. Secondarily, do fern
species show significant differences in functional traits?
In answering these questions, it is hoped that a clearer mechanism for fern species80
distribution in the Catlins will be revealed. Should significant environmental trait
differences be seen between tree-type defined forest sites, the habitat heterogeneity model
for species coexistence would have support. However, failing to find such differences
prompts a closer examination of the fern species themselves – do individual species give
significantly different functional trait measures? Coexistence of species with different85
functional strategies in a relatively homogenous environment would favour the functional
trait diversity hypothesis of community composition.
The environmental variables were measured at the fern sampling sites (differing by tree
type) to look for a heterogeneous pattern that may dictate fern species distribution. Also,
functional traits for several common fern species were analysed to gauge interspecific90
diversity. Subsequent statistical analyses intended to identify whether environmental
factors or functional traits appeared to more strongly influence fern species distribution.
2. Materials and Methods
Sampling was carried out along Old Possumer’s Track, through mixed native forest of
Tahakopa Bay in the Catlins, Otago. Additional sampling took place in similar forest95
surrounding Tautuku Outdoor Education Centre (TOEC), also in this region.
2.1. Environmental trait measurement
An initial species richness survey identified commonly occurring fern species and
allowed refinement of field techniques. At Tahakopa Bay, a random number table was
used to determine the number of paces along the track and the number of paces off the100
track that the study’s 24 quadrats were laid. At each point off the track, the nearest suitable
site with the desired tree type was located – angiosperm, gymnosperm or no tree (control).
) were laid, and tree type and species were noted.
Sub-litter soil was sampled from each quadrat for pH analysis and PVC soil collars (10cm
diameter) were planted in the centre of 15 quadrats (approx. 10cm deep). After a four day105
in-ground period, soil collars were fitted with a 10cm accumulation chamber (connected
to LI-8100 analyser) to measure soil respiration. Measures of average soil temperature
and CO2 flux were taken directly from analyser output, while Volumetric Water Content
(VWC) was calculated using Soil Moisture Probe Converter V6 (LI-COR Biosciences
Inc., available at https://licor.app.box.com/s/zysh30cjyg5pqxexkfkm). Soil samples110
(20mL) were finely ground, mixed with 20mL filtered water and measured with a pH
glass electrode once sediment settled. A Plant Canopy Analyser (LAI-2200C; LI-COR
Biosciences Inc., Lincoln, NE, USA) was used to measure canopy Leaf-Area Index (LAI)
– the leaf area per unit ground area (Jordan, 1969) – at 1.5m above the ground.
Within each quadrat, all present fern species were recorded, as well as abundance of115
individuals. Any epiphytic species present on the tree associated with each quadrat
(though outside of the quadrat) was also noted. The most abundant species were identified
and six species were selected for functional trait measurement.
2.2. Functional trait measurement120
Fern individuals were measured in the field or sampled for subsequent laboratory
analysis. Sampling was across a wide area to avoid selecting closely related individuals.
Species Asplenium flaccidum*, Asplenium hookerianum, Blechnum discolor,
Hymenophyllum bivalve*, and Microsorum pustulatum* were sourced from forest
neighbouring TOEC (*=epiphytic; Brownsey & Smith-Dodsworth, 2000). Leptopteris125
hymenophylliodes was not present at TOEC – sampling and measurement of this species
took place at Tahakopa Bay.
To determine Specific Leaf Area (SLA), 2 fronds were sampled from 10 individual ferns
per species. Samples were photographed in a digital scanner and surface area calculated
by ImageJ software analysis (Rasband, 1997). Root samples (100mm length) were130
collected from 3 individuals per species, thoroughly washing to remove sediment, and
digitally scanned for IJ_Rhizo analysis (ImageJ macro) to compute Specific Root Length
(SRL) (Pierret et al., 2013). Pinnae thickness measurements for 10 individuals per species
were taken in vivo with electronic callipers.
Frond gas exchange measurements in the field used a portable gas-exchange analyser135
system and leaf chamber fluorometer (LICOR-6400XT; LI-COR Biosciences Inc.,
Lincoln, NE, USA). Readings were taken in vivo from three individuals per species. The
rates of transpiration (T) and net photosynthesis (A) measurements were used to calculate
instantaneous Water Use Efficiency (WUE=A/T; ratio of CO2 fixation to water loss
through transpiration) for individual ferns (Karaba et al. 2007). Each frond area analysed140
in the leaf chamber was scanned using ImageJ; area values were used to adjust net
photosynthesis rate (A) and Photosynthetically Active Radiation (PAR) measurements
from fern gas-exchange analysis. Light Response Curve Fitting 1.0 tool (available at
http://landflux.org/Tools.php), used these measurement to estimate Light Compensation
Point (LCP) and maximum net assimilation rate (Amax), and produce light response curves145
for individuals of each species.
2.3. Data Analysis
Data analyses were carried out using RStudio software (RStudio, Inc., Boston, MA,
USA). The differences in fern traits (SLA, SRL, pinnae thickness, WUE, LCP and Amax)
between species were analysed through single-factor ANOVA using the linear model150
procedure. Species were considered to show statistically significantly differences with a
p-value below 0.05. Post-hoc analysis involved multiple-comparison tests between
species, using Tukey’s HSD method (α=0.05). Differences in environmental variables
(LAI; soil pH, temperature, CO2 flux and VWC) between tree-type characterised sites
were similarly analysed. For all fern traits and environmental factors, Levene’s tests155
showed that data met the assumption of homoscedasticity (P>0.05). Boxplot figures for
significant fern traits and photosynthetic light response curves were produced in RStudio.
3.1. Environmental traits
The mean soil temperature was found to differ significantly between tree-type160
characterised sites (F(2,12)=6.2505, P<0.05). Post-hoc analyses showed that the mean soil
temperature at gymnosperm tree sites was significantly higher than at sites with no tree
(Tukey’s HSD, P<0.05). No significant differences were detected for the LAI or the pH,
CO2 flux or VWC of soil between tree-type characterised sites.
3.2. Fern traits165
The sampled species had significantly different SLA (F(5,114)=16.55, P<0.001), SRL
(F(5,23)=12.84, P<0.001), pinnae thickness (F(5,54)=73.98, P<0.001) and WUE
(F(5,12)=43.65, P<0.001) measurements. A. flaccidum and B. discolor showed significant
differences from all other species in all assessed functional traits. All species showed
significant differences from each other in SLA and pinnae thickness, with pinnae170
thickness results statistically significant at 99.9% level for all species (Table 1.). The LCP
and Amax did not differ significantly between species.
3.2.1. Specific Leaf Area
Compared to other species, A. hookerianum had a significantly larger SLA (Tukey HSD,
P<0.001) (Fig. 1). The lowest SLA measurements were taken from A. flaccidum;
measurements were significantly lower than those of A. hookerianum (Tukey’s HSD,
P<0.001) and M. pustulatum (Tukey’s HSD, P<0.01). There was insufficient evidence180
favouring exclusion of the outlying value for A. flaccidum in Figure 1; it was deemed a
feasible measurement and retained.
Figure 1. Specific Leaf Area (SLA) measurements for fern species A.
flaccidum (ASPfla), A. hookerianum (ASPhoo), B. discolor (BLEdis), H.185
bivalve (HYMbiv), L. hymenophylloides (LEPhym) and M. pustulatum
(MICpus) in mm2
. Plots show median value (bold horizontal line), 1st
quartile, and 95th
percentile of median. Different letters indicate
significant differences between species according to Tukey’s HSD at
P<0.05. N(per species) = 20.190
3.2.2. Specific Root Length
M. pustulatum gave the highest SRL measurements – significantly higher than those of
other species, except A. flaccidum (Tukey’s HSD, P<0.01) (Fig. 2). There was insufficient195
evidence in favour of exclusion of the outlying value for A. flaccidum, which is likely
responsible for the lack of significant difference between the SRL measurements of this
species and M. pustulatum. This outlier, and one associated with A. hookerianum, were
deemed feasible measurements and retained. An outlier for M. pustulatum was not
considered inaccurate and it was removed.200
The lowest SRL measurements were taken from L. hymenophylloides; these
measurements only differed significantly from those of A. flaccidum (Tukey’s HSD,
P<0.01) and M. pustulatum (Tukey’s HSD, P<0.001).
Figure 2. Specific Root Length (SRL) measurements for fern species A.205
flaccidum (ASPfla), A. hookerianum (ASPhoo), B. discolor (BLEdis), H.
bivalve (HYMbiv), L. hymenophylloides (LEPhym) and M. pustulatum
(MICpus) in mg-1
. Plots show median value (bold horizontal line), 1st
percentile of median, and outliers (open circles). Different
letters indicate significant differences between species according to210
Tukey’s HSD at P<0.05. N(per species) = 5.
3.2.3. Pinnae thickness
The pinnae thickness of A. flaccidum was significantly greater than that of other species
(Tukey’s HSD, P<0.001), whereas H. bivalve and L. hymenophylloides both had
significantly thinner pinnae (Tukey’s HSD, P<0.001) (Fig. 3). There was insufficient215
evidence favouring exclusion of the outlying values for A. flaccidum and H. bivalve in
Figure 3; they were deemed a feasible measurements and retained.
Figure 3. Pinnae thickness measurements for fern species A. flaccidum
(ASPfla), A. hookerianum (ASPhoo), B. discolor (BLEdis), H. bivalve220
(HYMbiv), L. hymenophylloides (LEPhym) and M. pustulatum (MICpus)
in mm. Plots show median value (bold horizontal line), 1st
percentile of median, and outliers (open circles). Different letters
indicate significant differences between species according to Tukey’s
HSD at P<0.05. N(per species) = 10.225
3.2.4. Water Use Efficiency
WUE of ferns varied greatly between species. WUE of M. pustulatum was significantly230
higher than other species (Tukey’s HSD, P<0.005), while the WUEs of H. bivalve and L.
hymenophylliodes were notably lower, and were together significantly different from all
other species except A. flaccidum (Tukey’s HSD, P<0.01) (Fig. 4).
Figure 4. Water Use Efficiency (WUE) measurements for fern species A.235
flaccidum (ASPfla), A. hookerianum (ASPhoo), B. discolor (BLEdis), H.
bivalve (HYMbiv), L. hymenophylloides (LEPhym) and M. pustulatum
(MICpus) in mol CO2 mmol H2O-1
. Plots show median value (bold
horizontal line), 1st
quartile, and 95th
percentile of median.
Different letters indicate significant differences between species240
according to Tukey’s HSD at P<0.05. N(per species) = 3.
3.2.5. Photosynthetic light response
The photosynthetic light response of each species followed a similar curve – rapidly
increasing photosynthetic capacity at low photon flux densities, followed by saturation of245
photosynthetic capacity at higher flux densities (Fig. 5). The maximum photosynthetic
capacities of H. bivalve and L. hymenophylliodes are lower than other species. However,
analysis of the ferns’ maximum net assimilation rate (maximum rate at which
photosynthesising fronds fix carbon) and Light Compensation Point (light intensity when
photosynthetic and respiration rates are equal) – derived from light response curves for250
individual samples – revealed that no species differ significantly at the 0.05 level.
Figure 5. Effect on photosynthetic capacity (molCO2 m-2
frond area s-1
increasing photon flux density (molphotons m-2
frond area s-1
) in fern species
A. flaccidum (ASPfla), A. hookerianum (ASPhoo), B. discolor (BLEdis),255
H. bivalve (HYMbiv), L. hymenophylloides (LEPhym) and M. pustulatum
(MICpus). Values plotted are averaged from 3 samples per species.
The present study sought to determine the prevailing mechanism of fern coexistence in260
Catlins’ forest. The forest environment showed little differentiation between tree-type
characterised sites. The diverse fern community persists in spite of this, and analysed
species showed significant interspecific differences in functional traits. Hence, of the
proposed community diversity mechanisms, functional trait diversity appears to prevail
over habitat heterogeneity.265
Most environmental traits were homogenous across tree-type characterised sites, with
only soil temperature differing significantly. However, soil temperature alone is not
considered to substantiate habitat heterogeneity. I would require further support through
other environmental differences to favour this mechanism.
There is support for the functional trait diversity model in significant differences found270
between species for the traits SLA, SRL, pinnae thickness and WUE.
High SLA confers superior photosynthetic ability (Bannister & Wildish, 1982),
evidencing a competitive advantage for A. hookerianum in this study. Significant
differentiation of this species from others in terms of SLA will contribute to the definition
of its niche and promotion of species coexistence.275
Previous work suggests that high SRL is linked to rapid-growth species, with this trait
positively related to respiration, plant nutrition, and growth of roots, (Roumet et al.,
2006). Hence, the functional significance of high SRL is that it allows efficient resource
exploitation, essential for short life cycles (Roumet et al., 2006). Applying this to the
present study, we might infer that M. pustulatum may coexist with potential competitors280
with its distinct “fast-living” strategy, enabled by functional trait diversity.
Water regime notably influences fern distribution (Karst et al., 2005), it is therefore
unsurprising that WUE reportedly influences species habitat preference (Parra et al.,
2009). High WUE is advantageous when water is limited (Bacon, 2004), suggesting
water-efficient M. pustulatum would favour drier microsites – growing conditions of this285
epiphytic species likely offer less moisture than the forest floor. Niche heterogeneity is
achieved by this species through notably high WUE, and this unique resource use will
minimise interspecific competition. Similarly, the low WUE of H. bivalve and L.
hymenophylloides will contribute to niche differentiation of these species.
The pinnae thickness has been related to WUE (Johnson et al., 2000); the functional value290
of thick pinnae is tolerance of stressful conditions (Kluge & Kessler, 2011). My results
give further evidence that the coriaceous M. pustulatum and filmy H. bivalve and L.
hymenophylloides, with their respective high and low WUEs, show niche heterogeneity.
A. flaccidum had the thickest pinnae, demonstrating a means for this species to differ from
others in resource use, potentially minimising competition. Interestingly, A. hookerianum295
(of the same genus) had the lowest SLA. Significant trait difference at genera-level in this
case supports functional diversity as a coexistence mechanism.
Nasrulhaq-Boyce and Mohamed (1987) applied ‘sun fern’ and ‘shade fern’ classifications
to species in their study; this approach appears valid in the present study, given the notable
partitioning of species by light response. Sun fern physiology allows higher300
photosynthetic capacity with light saturation, while shade ferns (with relatively low
chlorophyll content and stomatal density) photosynthesise efficiently at low irradiance.
The maximum photosynthetic capacities of H. bivalve and L. hymenophylloides were
notably lower than those of other species; we might differentiate this isolated pair into the
From these results, fern species specialisation into differentiated niches could be inferred,
with species distribution dictated by a microsite mosaic, as opposed to, and irrespective
of, dominant tree-type.
Having found little difference in the environmental traits between tree-type characterised
sites I conclude that tree type is not having a significant manipulative effect on fern310
community composition. Therefore, the habitat heterogeneity model is not favoured, and
with significant differences between species for the majority of fern functional traits there
is good support of the functional trait diversity model.
Previous studies have emphasised the wide scope for expanding fern ecology. Lehman et
al. (2002) highlighted the absence of literature addressing the role of interspecific315
competition in assembling fern communities, also inviting a comparison between this and
the effect of the ferns’ environment in their forest community structure. Recognising the
demand for such investigation is encouraging for the reception and value of this study.
Application of these findings may be to guide forest management strategies, with a view
to conserving the Catlins unique fern assemblage. Might specialised niches be restrictive320
for ferns if resource availability is altered or compromised in the future? Manipulative
experimentation in subsequent investigations may be worthwhile, to further
understanding of diversity maintenance and species’ responses to change.
Acknowledgements – I thank Melanie Oliver for her for partnership in researching and325
carrying out this study. I am grateful to John Steel, Bill Lee, Steve Higgins, Christoph
Matthaei, and Gregory Nelson for their guidance and advice as this study was prepared
and carried out, and to Edmund February and Tony Stumbo for technical assistance in the
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