Journal of Threatened Taxa | www.threatenedtaxa.org
| 26 June 2023 | 15(6): 23416–23424
ISSN 0974-7907
(Online) | ISSN 0974-7893 (Print)
https://doi.org/10.11609/jott.8249.15.6.23416-23424
#8249 | Received 01
November 2022 | Final received 12 May 2023 | Finally accepted 17 May 2023
Leaf defoliation and Tabernaemontana rotensis (Asterids: Gentianales: Apocynaceae) flower induction and fruit development
Thomas E. Marler
Bagong Kaalaman
Botanikal Institute, 15 Rizal Street, Barangay Malabañas, Angeles City 2009, Philippines.
Editor: Moses Fayiah, Njala University, Sierra Leone, western Africa. Date of publication: 26 June 2023
(online & print)
Citation: Marler, T.E. (2023). Leaf defoliation and Tabernaemontana rotensis
(Asterids: Gentianales: Apocynaceae) flower induction and fruit development. Journal of Threatened Taxa 15(6): 23416–23424. https://doi.org/10.11609/jott.8249.15.6.23416-23424
Copyright: © Marler 2023. Creative Commons Attribution 4.0
International License. JoTT allows unrestricted use, reproduction, and
distribution of this article in any medium by providing adequate credit to the
author(s) and the source of publication.
Funding: None.
Competing interests: The author declares no competing interests.
Author details: Thomas
Marler is a terrestrial ecologist who has conducted plant physiology research in Micronesia, Philippines, and
Thailand for more than 30 years.
Acknowledgements: I thank Gil Cruz and Maren Roe
for field assistance.
Abstract: Tabernaemontana
rotensis (Kaneh.) P.T.
Li is an attractive small tree that is endemic to the islands of Guam and Rota.
Conservation efforts of the threatened population are constrained by lack of
research. Understanding the ecology of flower and fruit development is
fundamental to successful conservation of threatened angiosperms. This study
determined the extent of flower induction following tropical cyclone
defoliation, tested the efficacy of 10% urea sprays as a defoliant to induce
flowering, and quantified the resulting fruit expansion to determine ontogeny
traits. A total of 512 inflorescences were observed, half following tropical
cyclones and half following defoliation with urea. Fruit length was measured
every five to seven days until seed dispersal. The mean length of time between
defoliation and initial flower anthesis was 29 days, and did not differ between
tropical cyclone defoliation and urea solution aerosol defoliation. Four stages
of observable fruit development were identified following anthesis. Linear
increases in ovary length occurred for two weeks, maximum ovary length occurred
at about day 30, color break from green to orange began at about day 60, and
seed dispersal occurred at about day 90. Defoliation treatment did not
influence the timing of these stages. The results indicated that tropical
cyclone and urea solution defoliation consistently generated mast flowering
after about one month with mast seeding about three months later.
Conservationists may use this new knowledge to predictably schedule seed harvests
at about four months following a natural or anthropogenic defoliation event.
Many Tabernaemontana species are exploited for
traditional medicine, and the use of defoliation to manipulate phenology of
these species may benefit the practitioners of this trade.
Keywords: Conservation biology, crop
regulation, defoliation, endangered plants, Guam, masting,
tropical cyclone.
Introduction
Of the world’s described tree
species, about 58% are endemics constrained to single countries (Beech et al.
2017). Islands contain many endemic species, representing taxa that are among
the most threatened globally (Caujapé-Castells et al.
2010). An ecological understanding of all aspects of reproductive biology is
required for development of effective conservation practices for threatened
endemic tree species, therefore, an understanding of the reproductive biology
of island species is of utmost importance for developing successful
conservation programs (Kaiser-Bunbury et al. 2010). Tabernaemontana
rotensis is restricted to two adjacent islands in
a single archipelago (USFWS 2015), with most of the population existing on the
single island of Guam (USFWS 2020). Protecting habitat of T. rotensis from ongoing land use change may not be enough
to recover the species, as knowledge of fruit set, fruit ontogeny, seed
quality, seed storage, and regeneration behaviors are also critical.
The native flora of the Mariana
Islands includes several Apocynaceae tree species,
including Tabernaemontana rotensis. The endemic range of the small tree includes
the islands of Guam and Rota, and the species was listed as threatened under
the United States Endangered Species Act in 2015 (USFWS 2015). The known global
population declined about 25% between the 2015 listing and the 2020
conservation status update for the species (USFWS 2020).
The primary threat to this tree
species has been identified as habitat loss and fragmentation due to land use
change (USFWS 2015). For example, an ongoing military construction program will
permanently convert more than 2,000 ha within northern Guam T. rotensis habitat (USFWS 2020). This Guam case study is
germane to contemporary global extinction risk factors, as land use change is
the greatest threat causing tree extinctions (BGCI 2021) and will remain a
major driver of plant extinctions into the future (Pereira et al. 2012).
Spatial patterns of the population reveal an allopatric distribution of several
sub-populations. For example, only three sub-populations contain at least 25
mature trees, and a reported 98% of these mature trees occur in a single
sub-population (USFWS 2020). This geographical clustering of the T. rotensis population adds to the extinction threats.
Endemic plants that are spatially constrained are generally faced with the
greatest extinction risks (Enquist et al. 2019; Nic Lughadha et al. 2020; Staude et al. 2020).
The forests of the Mariana
Islands are often disturbed by tropical cyclones (Stone 1971; Marler 2001). Masting events have
been observed in T. rotensis trees following
tropical cyclones, but this plant response has not been adequately investigated
to confirm its consistency. A full ecological understanding of this phenomenon
and the dynamic changes during fruit ontogeny would benefit conservation and
horticultural decisions.
Horticulturists are ideally
equipped to conduct pragmatic investigations aimed at understanding plant
ecology and improving conservation approaches (Marler
2017). The horticulture industry exploits horticultural defoliants for various
purposes, including inducement of flowering in some species. One commonly used
defoliant for managing guava trees, for example, is urea aerosol sprays with
concentrations of 3% to 30% (Chapman et al. 1979; Singh et al. 2002, 2018; Samant et al. 2020).
Tabernaemontana rotensis responds well to horticultural
management and serves as an attractive urban landscape tree. Trees in managed
gardens in Guam and Philippines and several in situ locations in Guam provided
the experimental sites for this study. The objectives were to confirm the
extent and timing of mast flowering after tropical cyclones, determine if urea
leaf sprays could generate defoliation that induced mast flowering, then
measure fruit development from anthesis to the seed dispersal stage for the two
defoliation sources. I hypothesized that urea solution defoliation of T. rotensis trees would elicit mast flowering and fruiting
in a manner similar to tropical cyclone defoliation. The new knowledge will
directly inform conservation decisions.
Materials
and Methods
Study Locations
Northern Guam was used for all tropical
cyclone observations and three of the urea defoliation studies. The latitudinal
range was N13.493°–13.611°, and the longitudinal range was E114.837°–144.926°.
The elevation range was 74–180 m. Climate is classified as Köppen:
Af, with mean temperature of 27.7°C, mean monthly
rainfall of 19.8 cm, and mean relative humidity of 77.3%. The soils for the in
situ observations were primarily Clayey-skeletal, gibbsitic,
nonacid, isohyperthermic Lithic Ustorthents,
and the soils for the controlled urea spray study were Clayey, gibbsitic, nonacid, isohyperthermic,
Lithic Ustorthents.
The conservation research garden
in the Philippines was located at N15.165°, E120.505° at 234 m. Climate is
classified as Köppen: Am, with mean temperature of
29.7°C, mean monthly rainfall of 9.4 cm, and mean relative humidity of 82.7%.
The soils were Coarse loamy, isohyperthermic, Typic Untipsamment.
Flower Induction
Tabernaemontana rotensis trees on Guam were observed
following several tropical cyclone events to confirm the circumstantial
observations that indicated mast fruiting occurred in response to tropical
cyclones. These were Typhoon Tingting on 28 June
2004, Typhoon Chaba on 21 August 2004, Typhoon
Francisco on 16 October 2013, and Typhoon Dolphin on 15 May 2015. Disparity in
tree damage among habitats is a common feature of tropical cyclones, and
results from spatial differences in topography and forest structure (Marler et al. 2016; Zhang et al. 2022).
Data Collection
In order to include a control
treatment, various habitats were visited following each of these four tropical
cyclones to find habitats with T. rotensis
trees that were not defoliated. Eight trees that were defoliated and eight
trees that were not defoliated were visited beginning three weeks after each
tropical cyclone, then every three to four days thereafter until open flowers
were observed.
The trees that were not
defoliated did not exhibit any flower production throughout the dates of the
study. The trees that were defoliated rapidly exhibited flowers, and dates of
initial anthesis in each inflorescence were recorded for eight inflorescences
per tree for a total of 256 inflorescences for the entire investigation of
typhoon-defoliated trees. Characteristics of the four natural defoliation
replications are described in Table 1.
A solution of 10% urea was
sprayed as an aerosol over the entire canopy of eight in situ trees averaging
2.4 m in height in May 2012 as an initial test as a defoliant. Although most of
the leaves were damaged and many abscised in accordance with objectives, the
indiscriminate application also damaged stem apices such that vigorous
vegetative regrowth occurred from lateral buds. Eight trees with a mean height
of 2.7 m were sprayed in June 2012 by strategically spraying each stem by
beginning with the oldest leaves and continuing in an apical direction until
reaching the youngest fully expanded leaves. The remaining apical leaves were
not sprayed, but were pruned on each petiole with shears. This procedure
avoided damage to the stem apices with the urea solution, and copious
inflorescences were included in the regrowth. These eight trees served as the
first urea-defoliation replication for this investigation, and eight untreated
trees in the same habitat were included as controls. Characteristics of the
resulting four urea defoliation replications are described in Table 1. The
procedure was repeated with a second set of 16 in situ trees exhibiting a mean
height of 2.8 m in August 2012, with half of them serving as controls. In order
to confirm the efficacy of this treatment for inducing flowers in cultivation,
16 T. rotensis trees with a mean height of 2.6
m and growing in a border planting of a commercial farm in Dededo,
Guam were used as the third replication, with eight trees serving as controls.
The urea application was applied in September 2012. These trees were sourced
from a northeast Guam locality. Finally, 16 trees averaging 2.4 m in height and
growing in an Angeles City, Philippines research garden were used as a fourth
replication, with eight trees serving as controls. These trees were sourced
from the same Guam locality. The urea application was applied in September
2015.
The growth of all control trees
throughout the course of the study did not include any inflorescence
production. Each of the eight urea-defoliated trees within the four
replications were observed every three to four days to record leaf abscission
and regrowth responses. Dates of initial anthesis for eight inflorescences per
tree were recorded for a total of 256 inflorescences.
Fruit Development
Developing fruits from the
induced mast flowering events were observed and measured to more fully
characterize reproductive behavior of this endemic tree. Four in situ trees
following each tropical cyclone described in section 2.1 were selected for
naturally defoliated trees. Eight inflorescences per tree were marked and the
length of one fruit per inflorescence was measured. For each marked fruit, the
fruit length was measured to the nearest mm every five to seven days until seed
dispersal. Therefore, 32 fruits were observed for each defoliation replication
for a total of 128 fruits for the growth following tropical cyclone
defoliation. Four of the cultivated trees for each of the four events for the
urea-defoliated study in section 2.1 were used for observing fruit development
for horticulturally defoliated trees. Eight inflorescences from each tree were
selected, and one fruit per inflorescence was marked for the measurements. All
decipherable ontogeny events were observed and recorded.
Statistics
For flower induction data, the
number of days between the defoliation date and the initial flower anthesis for
an inflorescence was calculated from the calendar dates that were recorded.
Each defoliation event was treated as a replication. The number of days for the
64 inflorescences within one defoliation replication were averaged to calculate
the mean number of days for each replication. The differences between tropical
cyclone versus urea defoliation treatments were determine by t test, n =
4.
Fruit growth quantified as ovary
length as a function of time was fitted with non-linear regression, and every
ovary measured followed the model y = A(1-eBx) where y
signified fruit length and x signified days since anthesis. For each
defoliation replication, all data from the 32 inflorescences were combined and
the data were fitted individually per replication to obtain the values for A
and B in the regression model. Thereafter, the influence of defoliation
treatment on fruit ontogeny was determined by subjecting parameter A and
parameter B to t test, n = 4.
For fruit development, the number
of days between anthesis readily observable developmental events was recorded
for each observed fruit. These events included the date that linear ovary
extension ceased, the date that maximum ovary length occurred, the date that
color break from green to orange began, and the date the ovary split open for
seed dispersal. The mean of the 32 fruits for each of four defoliation
replications was calculated for each of the developmental stages. The influence
of defoliation treatment on each developmental event was subsequently
determined by t test, n = 4.
Results
The individual T. rotensis flower is attractive and the corolla is
comprised of five homogeneously distorted petals (Image 1A). Petals are
reflexed for most of their length, but are flat near the apex with undulating
margins.
Flower Induction
The four tropical cyclones that
served as defoliation events consistently generated regrowth within one to two
weeks. The trees that received urea sprays exhibited leaf damage within one day
and regrowth within one to two weeks. Observance of developing inflorescences
occurred within two to three weeks for both defoliation treatments (Image 1B).
Mast flowering with initial anthesis occurred within one month. Flowering
continued for several weeks depending on the size of the inflorescence (Image
1C). The first flower to reach anthesis required 28.9 ± 0.3 days after the
defoliation event, and was not influenced by defoliation treatment (t =
0.171, P = 0.433).
Fruit Development
At anthesis the two halves of the
T. rotensis ovary appear as if they are united
within the corolla, and they retain this appearance until about 8 mm in length.
At this stage, the entire corolla tube abscises intact, revealing one prominent
style and stigma. Immediately following this event, the ovary splits into two
distinct halves separated by an acute angle. The angle separating the two
halves increases until the halves are oriented directly opposite each other on
the pedicel at about one month following anthesis.
The pattern of fruit length as a
function of time was remarkably consistent among the replications and
defoliation treatments. Parameter A of the non-linear regression model did not
differ between the two defoliation treatments (t = 0.242, P =
0.408). Similarly, parameter B did not differ between the defoliation
treatments (t = 0.342, P = 0.372). Therefore, the data from all
replications in the study were represented by a single model (Image 2).
There were four observable
developmental events that were identified during fruit growth. The increase in
fruit length was linear immediately after anthesis, then growth increment
deviated from linearity by slowing down at about two weeks (Image 2, Stage A).
Defoliation treatment did not influence the timing of this ontogenetic trait (t
= 0.092, P = 0.465). The ovaries were bright green initially and did not
change in color until fruits reached maximum length at 29–34 days after
anthesis (Image 2, Stage B). The date of maximum fruit length was not
influenced by defoliation treatment (t = 0.293, P = 0.389). Fruit
color morphed from bright green to dull green during the second month of fruit
growth and a muted orange color break occurred 55─63 days after anthesis (Image
2, Stage C). The timing of this color break was not influenced by defoliation
treatment (t = 0.281, P = 0.394). Color development progressed
during the final month of fruit growth until a bright orange phenotype
characterized the fruits as they split open to expose seeds at 88─94 days after
anthesis (Image 2, Stage D). The window of time between anthesis and the
opening of the ovary to expose seeds was not influenced by defoliation
treatment (t = 0.461, P = 0.330).
Discussion
The timing of first anthesis
following defoliation and duration of each stage of fruit development exhibited
notable stability among the individual trees, experimental sites, seasons, and
years in this study. The results were consistent with the hypothesis that urea
solution defoliation would generate plant responses similar to tropical cyclone
defoliation. There was a remarkable stability in timing of reproductive
behavior. Anthesis began at one month after defoliation and seed dispersal
occurred at about three months after anthesis. The field work also revealed two
general observations. First, variation in mature ovary length of T. rotensis fruits appeared to be constrained, with most
ovaries maturing at 38–43 mm in length. The general observations of thousands
of fruits during this Guam study revealed that ovary diameter or circumference,
which were not directly measured, may be a more variable fruit trait. Second,
many angiosperms are plagued by vulnerability to fruit abscission at critical
developmental stages, a phenomenon called “June drop” for many fruit crops
(Rieger 2006). Tabernaemontana rotensis did not exhibit this ontogenetic trait, and
every flower that set fruit appeared to be able to support the developing ovary
to maturity.
Masting is a common behavior among some tree
species, and many benefits of masting to tree
regeneration and community assembly are understood (Koenig 2021). For T. rotensis, synchrony of flowering among many sympatric
trees appears to be associated with the seed masting
behavior. This synchrony may increase mate availability which may improve
out-crossing and increased the percentage of flowers that become pollinated.
More research is needed to determine if defoliation-induced flowering also
generates increased seed count per fruit and increased seed viability.
Masting behavior is often linked to
natural disturbances which synchronize population phenology (Vacchiano et al. 2021). Understanding how natural events
affect seed production may be challenging, but my findings indicated that
tropical cyclone defoliation events may consistently lead to mast fruiting of T.
rotensis about four months after the disturbance.
These findings illuminate a facet of the ecology of the region that may be
directly influenced by climate change factors, as most models predict greater
intensity of future tropical cyclones (Marler 2014).
The use of horticultural defoliation treatments that do not damage stem apices
also consistently generated masting after about four
months. This relatively fixed maturation duration may be exploited by
conservationists to schedule seed harvesting events by recording the date of
the natural or anthropogenic defoliation events, then scheduling fruit harvest
events after about four months.
Several avenues of further study
are warranted. First, a dose response curve of urea throughout the entire
published 3% to 30% concentration range (Chapman et al. 1979; Singh et al.
2002, 2018; Samant et al. 2020) may reveal the most
efficacious dosage for T. rotensis. An
inadvertent benefit from this horticultural protocol is the nitrogen that is
transferred to the soil along with abscised leaves may act as fertilizer.
Therefore, urea dosages that are greater than the minimum required for
defoliation may be beneficial as a conservation action. Second, tree size may
influence masting behaviors, especially for small,
young trees that may not produce seeds as consistently as large trees (Bogdziewicz et al. 2020b). The range in tree size was
purposefully constrained in this pilot study for logistical reasons. More
research may be warranted to determine if the masting
behaviors and timing of fruit ontogeny stages are consistent among a range of T.
rotensis tree size categories. Third, the
mechanisms of defoliation caused by urea are not fully understood, but likely
involve osmotic stress due to reduced osmotic potential on the laminae
surfaces. Productivity of this tree species is mostly limited by phosphorus
within in situ settings (Marler 2021). The use of
triple superphosphate solutions to impose laminae surface osmotic stress may
reveal a response similar to that of urea solutions. Studies designed to
determine dosage and efficacy may also reveal if translocation of phosphorus
from leaves to stems may occur prior to leaf abscission. If this is shown to
occur, the increased stem nutrient pool would be available for translocation
into post-defoliation regrowth. Fourth, numerous biology questions were beyond
the scope of this paper, and remain to be studied. These include all aspects of
pollination biology, histological changes of the ovary from fertilization
through seed maturation, and seed dispersal strategies. Fifth, the influences
of climate change on plant masting behavior are being
actively studied (Bogdziewicz 2022; Bogdziewicz et al. 2020a). The manner in which climate
change influences the reproductive behaviors of this tree species are not
known, but may be studied in the future using my findings as a historical
benchmark. The results herein illuminate the fact that disturbance of a forest
community by a tropical cyclone may provide some beneficial outcomes to some
species. Climate change predictions indicate more intensity of future tropical
cyclones (Marler 2001). The regeneration and
recruitment dynamics of native forests that are frequently subjected to tropical
cyclone disturbance may be unique when compared to forests in regions that do
not experience tropical cyclones (Chao et al. 2022). A comprehensive look at
the full spectrum of T. rotensis plant and
population responses to tropical cyclones may reveal many interesting aspects
of biology and ecology in the face of frequent large-scale disturbances.
This small, handsome Apocynaceae tree continues to be subjected to the
anthropogenic threats that caused the federal listing on the U.S. Endangered
Species Act (USFWS 2015). The habitat loss due to land use change (USFWS 2020)
will not subside in the foreseeable future because of the expansive military
buildup occurring on Guam (Marler 2013). Formal
recovery programs for endangered tree species depend on experimental and
observational studies to provide knowledge to inform conservation decisions.
The current study adds to a growing body of horticultural and ecological
literature on this species. The seeds of T. rotensis
rapidly lose viability during storage in ambient conditions, and respond well
to full sun as germination and seedling growth conditions (Marler
et al. 2015). The CO2 efflux from T. rotensis
stems exhibits a pattern that is dependent on the diel cycle, and is greatest
during the photoperiod at about 2.5 µmol·m−2·s−1 and
least during the nocturnal period at about 1.5 µmol·m−2·s−1
(Marler & Lindström
2020). Green and senesced leaves of T. rotensis
contain relatively high magnesium, manganese, and nickel concentrations in
comparison to 24 sympatric plant species (Marler
2021). Leaf nutrient resorption and senesced leaf traits indicate that T. rotensis leaf litter is relatively labile, with more
rapid decomposition and nutrient turnover predicted than for most of Guam’s
sympatric species (Marler 2021).
The genus Tabernaemontana
contains about 100 described species growing in tropical and subtropical
latitudes (Silveira et al. 2017). Although a considerable amount of research
has been devoted to the genus, the focus has been on pharmacological properties
of the plant organs (Naidoo et al. 2021). As a result, horticulture, ecology,
and conservation questions have not been adequately answered. In the absence of
research on a species of interest, the use of surrogate taxa for research may
provide valuable information (e.g. Marler et al.
2021). Therefore, my findings on masting behaviors
and fruit development may inform management decisions for other closely related
Tabernaemontana species. The extensive
literature on phytochemicals and ethnomedicinal uses of Tabernaemontana
species provides a potential avenue for expanding the conservation efforts of T.
rotensis. The closely related Tabernaemontana
pandacaqui Lam. is among the species that have
been studied for its medicinal value (Taesotikul et
al. 1990). Medicines extracted from trees are integral to the well-being of
millions of people, and research on this aspect of tree value is critical for
decision-makers to understand the urgent need for conserving the world’s trees
(Rivers et al. 2022). Therefore, a dedicated research program focused on
identifying the medicinal uses of T. rotensis
has potential for successful outcomes and may add justification for convincing
decision-makers about the value of conserving this island endemic tree. There
is a sense of urgency to this goal, as the known global T. rotensis population declined about 25% between 2015 and
2020 (USFWS 2020).
Conclusion
Defoliation of T. rotensis trees caused synchronized inflorescence
production with anthesis occurring after about one month, maximum fruit length
after about two months, color break of pericarp tissue from green to orange
after about three months, and seed dispersal after about four months. Tropical
cyclones provide the main source of natural defoliation within the endemic
range of the species, and climate change may alter regeneration and recruitment
behaviors of this tree species via the predicted changes in tropical cyclone
intensity. An aerosol spray of urea solution provided the experimental source
of defoliation, with plant responses that were similar to tropical cyclone
defoliation. Conservationists may use this new knowledge to manually induce
mast flowering events and accurately predict mast seed production windows of
time following natural and anthropogenic defoliation. This benefits conservation
projects designed to salvage plants from a planned construction site because
practitioners can use this knowledge to force scheduled seed production rather
than wait for a natural flowering event.
Table 1. The influence of
defoliation of Tabernaemontana rotensis in Guam and Philippines on flower induction
(eight trees per replication, eight inflorescences per tree) and fruit growth
(four trees per replication, eight fruits per tree).
|
Defoliation replication |
Date |
Location |
Community type |
|
Natural defoliation events |
|
|
|
|
Typhoon Tingting |
vi.2004 |
Guam |
in situ |
|
Typhoon Chaba |
viii.2004 |
Guam |
in situ |
|
Typhoon Francisco |
x.2013 |
Guam |
in situ |
|
Typhoon Dolphin |
v.2015 |
Guam |
in situ |
|
Urea defoliation events |
|
|
|
|
Forest trees |
vi.2012 |
Guam |
in situ |
|
Forest trees |
viii.2012 |
Guam |
in situ |
|
Agroforestry |
ix.2012 |
Guam |
circa situ |
|
Research garden |
ix. 2015 |
Philippines |
ex situ |
For
images - - click here for full PDF
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