Ecology of seed germination in threatened

trees: a review

Viheno Iralu, Humayun Samir Ahmed

Barbhuyan & Krishna Upadhaya

Energy, Ecology and Environment

ISSN 2363-7692
Volume 4
Number 4

Energ. Ecol. Environ. (2019) 4:189-210

DOI 10.1007/s40974-019-00121-w

1 23
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 Author's personal copy
Energ. Ecol. Environ. (2019) 4(4):189–210
https://doi.org/10.1007/s40974-019-00121-w
REVIEW PAPER
Ecology of seed germination in threatened trees: a review
Viheno Iralu1 • Humayun Samir Ahmed Barbhuyan2 • Krishna Upadhaya3
1
Department of Environmental Studies, School of Human and Environmental Sciences, North-Eastern Hill University, Shillong 793 022, India
2
Department of Botany, School of Life Sciences, North-Eastern Hill University, Shillong 793 022, India
3
Department of Basic Sciences and Social Sciences, School of Technology, North-Eastern Hill University, Shillong 793 022, India
Received: 4 January 2019 / Revised: 13 May 2019 / Accepted: 29 May 2019 / Published online: 11 June 2019
Ó The Joint Center on Global Change and Earth System Science of the University of Maryland and Beijing Normal University 2019
Abstract The future of many tree species is at risk due to
the rapid decline of the world’s forests, over-exploitation
for timber, seeds, oils, resins, fruits and bark. In addition,
seed germination in many threatened species is convoluted
due to various physical factors such as moisture, light and
the presence of thick seed coat as well as physiological
factors such as seed dormancy. Studies pertaining to seed
germination, storage behaviour, dormancy-breaking tech-
niques, particularly of threatened tree species at global
level are limited. Therefore, the present study was con-
ducted to assess the progress made in the field of seed
germination as well as the challenges that exist in the
regeneration of such species that are of conservation value.
The results obtained from the analysis of 78 threatened tree
species showed that moisture is a critical factor for recal-
citrant seeds, while species with orthodox seeds require a
pre-treatment for breaking dormancy. Although most of the
studies on dormancy-breaking techniques have demon-
strated the effectiveness of one or two methods on seed
germination, a combination of treatments as well as use of
plant growth regulators improved the ability of seeds to
germinate. Water, light, nutrients and a favourable sub-
stratum are major regulatory factors that affect germina-
tion, growth and establishment of tree species. The findings
emphasize the need to develop guidelines for proper seed
handling and understand germination protocols necessary
for ecosystem management that would aid both in main-
taining biodiversity values and conservation of threatened
species.
& Krishna Upadhaya
upkri@yahoo.com
Keywords Disturbance
Dormancy
Growth regulators

Scarification
Treatments
1 Introduction
Trees constitute one of the most valuable components of
the world’s biodiversity. They have ecological, cultural and
economic values and are vital to the well-being of people
all around the world (Oldfield et al. 1998). Estimates of
global tree species richness range from 60,000 (Grandtner
2005) to 100,000 taxa (Oldfield et al. 1998), approximating
to about 15–25% of the 350,000–450,000 vascular plants of
the world (Scotland and Wortley 2004; Petit and Hampe
2006). However, since the dawn of human settlement,
many species have been subjected to various pressures
(Atkinson and Cameron 1993) not only because of global
climate change and land-use intensification, but also due to
an increase in biosecurity challenges (Meurk and Hall
2006). Anthropogenic activities have brought about 10% of
the world’s tree species close to the brink of extinction
(Oldfield et al. 1998). According to the Intergovernmental
Panel on Climate Change (IPCC), roughly 20–30 percent
of vascular plants and higher animals on the globe are at
the risk of extinction as temperatures increase by 2–3 °C
(Parry et al. 2007). It is very likely that even modest losses
in biodiversity would cause consequential changes in
ecosystem services (Parry et al. 2007; Seppälä et al. 2009).
Timber exploitation is the major menace to the rapid
decline of tree species. The rate of exploitation far exceeds
the period of regeneration forcing many common species to
become rare and threatened. In addition to habitat degra-
dation, fragmentation and over-exploitation, many of the
rare and threatened species such as Gymnacranthera
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canarica (King) Warb. (Keshavachandra and Krishnaku-
mar 2016), Hyophorbe lagenicaulis (L.H.Bailey)
H.E.Moore (Wood and Pritchard 2003), Magnolia dealbata
Zucc. (Corral-Aguirre and Sanchez-Velasquez 2006) and
Magnolia schiedeana Schltl. (Vásquez-Morales and Sán-
chez-Velásquez 2011) have restricted distribution and low
populations size and are, therefore, at a high risk of
extinction. The species that are represented by small pop-
ulations and poor adaptability thus warrants prioritization
as major categories in biodiversity conservation (Paal
1998). In this regard, the Convention on International
Trade in Endangered Species of Wild Fauna and Flora
(CITES) Timber Working Group (TWO) was formed at the
ninth Conference of the Parties (COP) for sustainable
management of internationally traded timber species. In
India, the export of Santalum album L. has been banned
(IUCN 2016). There are a number of studies that have
assessed and established the impact of industrialization on
the loss of vegetation and forest degradation (Ahmed 2008;
Yildirim et al. 2009). Oldfield et al. (1998) listed 7388 tree
species that have been evaluated as globally threatened.
Propagation of trees most commonly occurs through
seeds as they are the carriers of genetic resources for
species biodiversity, ecosystem restoration, conservation
and domestication (Berjak and Pammenter 2004). As a
result, in recent years, seed germination studies have
emerged as an important tool for conservation of species.
Seed germination studies help in understanding the causes
of species decline, persistence or spread in changing
landscapes (Schütz 2000). However, seed germination in
many threatened trees is convoluted due to seed dormancy.
In addition, viability and storage requirements of seed in
many species are unknown, making it difficult for ex situ
germplasm conservation. The knowledge on the germina-
tion, storage behaviour and ecological requirements of
many of the threatened trees remains unexplored and is a
prerequisite for any conservation initiatives.
Seed production, dispersion, predation and germination
are ecological processes, which affect the maintenance of
the populations and their colonization in space and time
(Alexander et al. 2001; Baskin and Baskin 1998; Lorente-
Adame and Sánchez-Velásquez 1996). Fragmentation and
habitat loss have adverse effects on these processes.
However, the effects of forest fragmentation on pre-dis-
persal seed predation have been poorly addressed in trop-
ical and subtropical forests (Cascante et al. 2002; Chacoff
and Aizen 2006). It is evident that there is low abundance,
diversity and species richness of seed predators in small
fragments due to environmental fluctuations (Didham
1997; Baguette and Schtickzelle 2003; Chacoff and Aizen
2006).
Although a number of studies on seed germination are
available from different parts of the world, information
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V. Iralu et al.
about their ecology such as patterns of dispersion, germi-
nation and establishment are scattered. The present paper
brings together the information on the germination studies
with special reference to globally threatened trees. Trees
that fall under the various threat categories of the IUCN
Red list (IUCN 2016) and ‘the world list of threatened
trees’ (Oldfield et al. 1998) were considered. The objective
of the study was to evaluate whether sufficient efforts have
been put forth for recovery of such species worldwide in
order to prevent them from extinction in nature through
seed germination. Seed storage behaviour, dormancy-
breaking techniques and factors responsible for the decline
of germination of such threatened trees have also been
reviewed.
2 Results and discussion
The present review includes a total of 78 species belonging
to 64 genera and 33 families. These include 69 angios-
perms belonging to 56 genera and 30 families. There were
nine gymnosperms belonging to eight genera and three
families. Fabaceae with 12 species and Magnoliaceae (10
species) were the dominant families followed by Diptero-
carpacea (6 species) and Cupressaceae (4 species). Of these
nine species are categorized as critically endangered, 19 as
endangered and 26 vulnerable (‘‘Appendix’’ section).
Twenty-eight species including Abies religiosa (Kunth)
Schltdl. & Cham., Dipterocarpus grandiflorus (Blanco)
Blanco, Horsfieldia pandurifolia H. H. Hu, Magnolia
punduana (Hook. f. & Thomson) Figlar, Pilgerodendron
uviferum (D. Don) Florin, Prosopis alba Griseb., Prunus
africana (Hook.f.) Kalkman, Swietenia macrophylla King,
Taxodium mucronatum Ten. were on the decline due to
rampant timber extraction and seven species including
Boswellia ovalifoliolata N. P. Balakr. & A. N. Henry, H.
pandurifolia, Ilex paraguariensis A. St.-Hil., Illicium
griffithii Hook. f. & Thomson, Magnolia officinalis Rehder
& E. H. Wilson, Myristica dactyloides Gaertn., Saraca
asoca (Roxb.) Willd., Sapindus oahuensis Hillebr. ex
Radlk., Symphonia globulifera L. f., were subjected to
over-extraction as non-timber forest products (NTFPs) in
the form of leaves, fruits, seeds, etc., owing to their
medicinal properties, thus hindering their natural regener-
ation. Species such as P. africana and Pterocarpus san-
talinus L.f. are highly exploited for timber as well as their
medicinal value (‘‘Appendix’’ section).
The distribution of the 78 tree species considered in the
present study revealed that 63 species were tropical, 13
subtropical and 6 temperate. Riparian, riverine, scrub and
subalpine were poorly represented in the list with one
species each (‘‘Appendix’’ section). Region-/country-wise
distribution of the species showed that India (17 species)
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Ecology of seed germination in threatened trees: a review
and China (14 species), the two most populated countries
of the world, top the list followed by South America (11
species), Africa (10 species), Mexico (9 species) and
Malaysia and USA (6 species each). The rest of the 12
countries had either one or two species each (Fig. 1).
However, in the present analysis, countries like Australia,
Philippines and Indonesia were poorly represented (‘‘Ap-
pendix’’ section). A critical analysis of the threats operating
on the species considered in the present paper revealed that
timber extraction, habitat degradation, poor regeneration,
low population and land-use change were the major threats
responsible for the decline of these species (‘‘Appendix’’
section).
2.1 Sexual reproduction and fruit type
Sexual reproduction and seed set in species are affected by
dicliny either monoecy or dioecy. A single tree could have
flowers with both fully functional male and female parts
(cosexual, bisexual, perfect, or hermaphroditic) or could
Fig. 1 Number of species in
different regions/countries
considered in the present study
191
also generate only male (‘‘andro’’) or female (‘‘gyno’’)
functional parts, but not both. In addition, any tree might
produce only cosexual, male, or female flowers, in any
combination (Coder 2008). Of the 78 species reviewed in
the present study, cosexuality was exhibited exclusively by
angiosperms (41species), a vast majority of which belon-
ged to Fabaceae (10 species) followed by Magnoliaceae (7
species) and Dipterocarpaceae (6 species), while dioecy
was exhibited by 19 angiosperms and 2 gymnosperms and
monoecy was present in 9 angiosperms and 7 gym-
nosperms. Dioecious species grow more slowly than
cosexual taxa as they are unable to self-pollinate and
require another individual for seed production (Schlessman
et al. 2014; Xia et al. 2013; Öster and Eriksson 2007). For
such plants, pollinator plays an important role in seed
production (Vamosi et al. 2006). The flowers of Olearia
hectorii Hook. f. are mostly perfect, i.e. have functional
male and female elements, and are probably insect-polli-
nated. Light partly controls reproductive vigour, because
shaded limbs and trees produce few flowers, whereas full
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light initiates abundant flowering (Rogers 1996). However,
43% of angiosperm families have dioecious members
(Renner 2014; Renner and Ricklefs 1995), prevalent
mostly in tropical or island flora as compared to the global
proportion of 6% (Queenborough et al. 2009; Vary et al.
2011). The taxonomical and geographical ubiquity of
dioecious species suggests that they compensate for their
reproductive disadvantages through ecological traits that
allow them to coexist with cosexual competitors. On the
other hand, monoecious trees separate genders into dif-
ferent flowers within the same individual tree to minimize
selfing. Wind-dispersed seeds and temperate zone climates
are associated with monoecy (Ohya et al. 2017).
In terms of fruit type, dioecious trees have large, fleshy,
single-seeded fruits that are dispesed by animals, as evident
by the presence of 10 dioecious and nine cosexual species
exhibiting drupe/berry fruits (‘‘Appendix’’ section). How-
ever, monoecious trees tend to exhibit cone type fruit as
observed in seven species. Fruit dispersal syndromes of the
studied species showed that majority were zoochorous (29
species) and 17 species were anemochorous. In gym-
nosperms, anemochory was the major dispersal syndrome
(8 species).
2.2 Seed set and seed banks
Threatened species are often characterized by small pop-
ulation of mature individuals and reduced seed production
(Fischer and Matthies 1998; Luijten et al. 2000). Plants
with zoochoric mode of dispersal are particularly affected
by disturbances resulting in decreased pollen availability
and reduced seed set (Jennersten 1988; Lamont et al. 1993;
Ågren 1996). Limited seed production in Magnolia stellata
(Siebold & Zucc.) Maxim. was attributed to elevated pollen
scarcity and genetic deterioration thus warranting manual
cross-pollination to maintain the population (Hirayama
et al. 2005). Similarly, in Talbotiella gentii Hutch. &
Greenway, the natural reproduction was affected due to
processes between pollen germination and fruit and seed
set, including pollen quality, fertilization rates, flower and
fruit abortion, and resource limitation (Dompreh et al.
2015). Microhabitats and disturbance also play an impor-
tant role in influencing seed production. For instance, in M.
dealbata, a high number of individuals were recorded in
secondary succession forest characterized by greater flower
and fruit production as compared to those in pasture lands
(Gutiérrez and Vovides 1997).
Seed banks are important sources of genetic reserves for
trees with semi-recalcitrant seed characteristics. The soil
seed bank is formed after viable seeds become buried in the
soil and litter, or accumulate on the ground surface
(Simpson et al. 1989). Soil seed banks of individual species
vary significantly in length from transient to persistent
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types (Thompson and Grime 1979; Thompson et al. 1997).
A persistent seed bank ensures the conservation of a spe-
cies as a fraction of seeds remains viable in the soil until
the next seed dispersal event, thus contributing to the
resilience of plant populations even when no seeds are
produced in a given year (Baskin and Baskin 1978; Baker
1989). This can even facilitate re-colonization after a local
extinction (Milberg 1994). Although many threatened trees
exhibit recalcitrant seed behaviour, they do not form per-
sistent seed banks as observed in Pinus sylvestris L. (Castro
et al. 2005), whereas certain other species such as M.
dealbata, M. schiedeana, M. punduana and Podocarpus
angustifolius Griseb. can form persistent seed banks in the
soil (Corral-Aguirre and Sanchez-Velasquez 2006; Vás-
quez-Morales and Sánchez-Velásquez 2011; Iralu and
Upadhaya 2016; Ferrandis et al. 2011). Buried seeds of M.
dealbata remained viable for 1 year (Corral-Aguirre and
Sanchez-Velasquez 2006) and that of M. schiedeana for
2 years (Vásquez-Morales and Sánchez-Velásquez 2011).
The persistence and viability of M. dealbata seeds was
however, limited by the availability of moisture (Corral-
Aguirre and Sanchez-Velasquez 2006) as also reported in
M. punduana (Iralu and Upadhaya 2016). Formation of
seed banks is essential for maintaining population viability.
Therefore, even in the case of lower seed production in a
given year as observed in Nothofagus glauca (Phil.)
Krasser (Burgos et al. 2008), the seeds in the soil can re-
establish and maintain the species population (Baskin and
Baskin 1978; Milberg 1994; Thompson et al. 1997).
However, a reduced seed bank on the forest floor due to
predation may affect the survival and mortality thus
resulting in reduced germination as observed in Phoebe
bournei (Hemsl.) Yen C. Yang, a threatened and endemic
species of China (Darong and Bosun 2001) as well as M.
schiedeana where seeds exposed to vertebrates resulted in
100% seed removal (Vásquez-Morales and Sánchez-
Velásquez 2011). Similarly, in N. glauca, the microlepi-
dopteran larva of Perzelia sp. is a pre-dispersal seed
predator that emerges from August to November and
coincides with the flowering of the species (Morales 1993;
Rojas 1996). The seeds are also attacked by post-dispersal
seed predators such as small mammals (Donoso et al.
2004). Swietenia macrophylla King. produces 40–50 win-
ged seeds per fruit on average and is classified as abundant
in terms of seed production. However, Lamb (1966) cited
seed predation by parrots and macaws, while they were still
on the trees and predation by different rodents on the forest
ground. The closed fruits on the ground were often attacked
by termites as well. In the seedling stage, the attack of
yellow caterpillars (Steniscadia poliophaea) that destroyed
the leaflets was common. Although the seeds, fruits and
seedlings present different predation forms, the
microlepidopter (Hypsipyla grandella Zeller) attacking the
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Ecology of seed germination in threatened trees: a review
apical branches was considered the major pest of S.
macrophylla. Thus, seed bank in the soil is dependent on
seed set frequency, disturbance, predation, persistence as
well as seed type that ultimately determine the regeneration
ability of the species.
2.3 Germination pattern
Following seed fall, the pattern of seed germination
determines the recruitment of species. Although germina-
tion studies have been conducted under laboratory or
controlled conditions, there is limited information from
field or natural conditions. Under natural environment,
seeds are dispersed across a wide variety of microhabitats
covering a range of abiotic and biotic conditions which
affects their germination (Castro et al. 2005). Once seeds
are dispersed, the various physical and biotic characteris-
tics, prevalent in the area act as a selective force in
determining which species will germinate and establish
(Bazzaz 1991). Germination under field conditions can be
spatially and temporally variable, as some microhabitats
may provide more favourable conditions than others
(Bisigato and Bertiller1999; Nilsson et al. 2000; Oleskog
and Sahlén 2000; Isselstein et al. 2002). Among environ-
mental factors, a suitable combination of temperature,
moisture and light conditions are considered as key deter-
minants of seed germination (Bewley and Black 1994;
Baskin and Baskin 1998). Raich and Khoon (1990)
investigated seed germination in a Dipterocarp forest under
three contrasting light conditions viz. forest understorey,
gap and clearing and reported that the critically endangered
D. grandiflorus and the endangered Vatica nitens King.
showed a germination percentage of 95% and 91% in forest
understorey and 33% and 5% in forest clearing, respec-
tively. A similar trend in germination was observed in
Aquilaria malaccensis Lam., Canarium littorale Blume.
and Shorea multiflora (Burck) Symington, with high ger-
mination in forest understorey. For, H. pandurifolia and
Litsea pierrei H. Liu, two endangered trees, germination
percentages of 28% and 54% in forest understorey and
17% and 21% in canopy gaps, respectively, were observed
in southwest China (Yu et al. 2008). Similarly, the criti-
cally endangered Shorea trapezifolia (Thwaites) P.S.
Ashton, a rainforest dipterocarp endemic to Sri Lanka, had
the highest germination of 83% in partial shade (de Zoysa
and Ashton 1991). There is a certain affinity of tree seeds
to germinate under shaded conditions. However, the seeds
of I. griffithii (Mukhia 2006) and Alstonia macrophylla
Wall.ex G.Don (Raich and Khoon 1990) exhibited germi-
nation percentages of 87% and 72% in forest gaps and
clearing and a low percentage of 3% and 27% in forest
understorey, respectively.
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Under natural conditions, the periodicity of rainfall
plays an important role in determining the germination
pattern of tree species. It also acts as a limiting factor for
seed production and seedling survival (Fischer and
Matthies 1998; Luijten et al. 2000). In A. malaccensis, seed
production was limited to the monsoon (June to August)
season (Tabin and Shrivastava 2014) while germination
was initiated in Ilex khasiana Purk. with the onset of few
showers of rain in spring (March–April) season (Upadhaya
et al. 2009). Seed moisture content is a major limiting
factor in recalcitrant seeds as germination percentage is
directly proportional to the seeds’ storage period. Bonner
(1990) classified seeds into: ‘true orthodox’ seeds that can
be stored for long periods at moisture contents of 5–10%
and sub-freezing temperatures; ‘sub-orthodox’ seeds that
can be stored under the same conditions, but for shorter
periods; ‘temperate recalcitrant’ seeds that cannot be dried
at all, but can be stored for 3–5 years at near-freezing
temperatures and ‘tropical recalcitrant’ seeds that also
cannot be dried, and they are killed by temperatures below
10–15 °C. However, some species exhibit semi-recalcitrant
characteristics when stored in appropriate conditions and
can remain viable for long periods, and they have been
classified as semi-recalcitrant type. Such seeds require a
moist substratum and specific storage temperatures. In
terms of storage behaviour, of the total 78 species con-
sidered in the present study, the seed type of 27 (35%)
species were not available while 23 (30%) species had
recalcitrant, 18 (24%) orthodox and 9 (12%) had semi-
recalcitrant seeds (‘‘Appendix’’ section).
Under controlled conditions, fairly high germination
percentages have been observed in some threatened trees
having recalcitrant and intermediate seeds. For instance, B.
ovalifoliolata germinated to a maximum of 70% (Savi-
thramma et al. 2012), A. malaccensis—92% (Tabin and
Shrivastava 2014), G. canarica—90% (Keshavachandra
and Krishnakumar 2016), Humboldtia laurifolia M.Vahl.—
80% (Jayasuriya et al. 2010), H. pandurifolia—90% (Yu
et al. 2008), Hyophorbe lagenicaulis (L.H.Bailey)
H.E.Moore—75% (Wood and Pritchard 2003), Myristica
malabarica Lam—100% (Kumar et al. 2002), S. globulif-
era—100%, (Corbineau and Côme 1989), S. asoca—80%
(Singh et al. 2005), Polylepsis besseri Hieron.—90%
(Gareca et al. 2012). Seeds of A. malaccensis failed to
germinate when stored for 15 days (Tabin and Shrivastava
2014). Seeds of G. canarica showed a maximum germi-
nation of 90% with an initial moisture content of 38% that
gradually declined after 70 days of storage (3% germina-
tion) when the moisture content reached 14% and failed to
germinate below this moisture level (Keshavachandra and
Krishnakumar 2016). Similarly, in Lophopetalum wight-
ianum Arn., the moisture content reduced to 9.21% after
30 days, and there was no germination, whereas at a
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194
moisture content of 16%, germination of 84% was
observed in L. wightianum (Keshavachandra et al. 2014). A
germination of 67% was observed in M. officinalis when
the soil water content was 25% (Shu et al. 2010; Zhou et al.
2012). Species vary significantly in their critical moisture
content that ranges between 12 and 31% (Ellis 1991;
Tompsett 1991). In Hopea odorata Roxb dehydration
below 24% inhibited germination (Corbineau and Côme
1989; Krishnapillay et al. 1991) and in H. pandurifolia,
50% of the seeds lost their ability to germinate when
moisture content reduced to 12% (Yu et al. 2008). Kumar
et al. (2002) reported 100% seed germination in M. mal-
abarica at moisture content of 27%. In M. dactyloides, the
critical moisture content was 34% (Sivakumar et al. 2006).
The seeds of Poeciloneuron pauciflorum Bedd. are a rare
and endemic tree species of the Southern Western Ghats of
India, which when stored at room temperature (28–31 °C)
exhibited critical moisture content of 22% for germination,
above which 70–75% seed germination was recorded while
germination decreased to 46–58% when the moisture
content dropped below 22% (Koilpillai 2017). The seeds of
Magnoliaceae such as Magnolia champaca (L.) Baill. ex
Pierre are known to be recalcitrant or short-lived orthodox
and require high moisture to maintain viability (Bahuguna
et al. 1987; Robbins 1988; Bisht and Ahlawat 1999). In
Swietenia mahagoni seeds stored at 2–5 °C with 4–5%
moisture content are viable up to 1 year (Schmidt and
Jøker 2000). In natural conditions, the depth of burial also
plays an important role in preserving seeds with semi-
orthodox characteristics as reported for M. schiedeana
(Vásquez-Morales and Sánchez-Velásquez 2011) and M.
dealbata (Corral-Aguirre and Sanchez-Velasquez 2006).
Thus, both environmental factors (light, moisture) as well
as seed storage behaviour are known to determine the
pattern of seed germination in tree species. Although par-
tial light and shaded conditions have been reported to be
favourable for some species, others have an affinity toward
forest gaps and clearings. In terms of storage behaviour,
recalcitrant seeds fail to germinate below a critical soil and
seed moisture content, whereas some species exhibiting
semi-recalcitrant characteristics when stored in appropriate
conditions can remain viable for long periods. Seeds of
Lysiloma acapulcense (Kunth) Benth., collected from four
sites in the tropical dry forest of Morelos, Mexico, showed
significant differences in seed size and germination among
provenances in the species. Germination capacity of stored
seeds (24 months) was still C 50% in all provenances
(Cervantes and Bonfil 2014).
2.4 Seed dormancy
Apart from the physical factors (moisture, light, substratum
etc.), seed dormancy contributes significantly to
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V. Iralu et al.
germination failure in many species (Bewley 1997). Baskin
and Baskin (1998, 2004) defined ‘dormancy’ as the phe-
nomenon by which seeds fail to germinate under conditions
otherwise considered as favourable for germination. While
many studies view seed dormancy as an obstacle in prop-
agation, it is, in fact, the adaptive mechanism that ensures
the survival of the species through periods of environ-
mental stress under natural conditions (Gutterman 1993;
Baskin and Baskin 1998; Garcı́a-Gusano et al. 2004; Ker-
mode 2005). Variation in dormancy between years has also
been suggested as an adaptation to unpredictable environ-
ments (Andersson and Milberg 1998). According to Phi-
lippi (1993), seed germination rate can be affected by
humidity levels during seed maturation with drier envi-
ronments inducing higher dormancy (Qaderi and Cavers
2000). The intensity of seed dormancy and degrees of intra-
specific variation depends upon several factors (Andersson
and Milberg 1998). Nikolaeva (1969, 1977) broadly clas-
sified seed dormancy under two general categories, i.e.
exogenous dormancy (i.e. outside the embryo) caused by
some physiological factors, characteristics of structures
including endosperm, seed coats, fruit walls, etc. (Niko-
laeva 1977; Yang et al. 2007) and endogenous dormancy
attributed to some characteristics of the embryo, the pres-
ence of the hard seed testa (morphological seed dormancy)
or germination inhibitors present in the capsules or endo-
sperm (Nikolaeva 1977; Hilhorst et al. 2006). Seed ger-
mination failure is attributed to the presence of either
factor. However, in some seeds, both endogenous and
exogenous seed dormancy may be present (Bewley and
Black 1994).
Physical and mechanical dormancy are the most com-
mon inhibitors of germination in many seeds. Families like
Leguminosae, Cannaceae, Malvaceae, Convolvulaceae and
Fabaceae exhibit exogenous dormancy due to an imper-
meable seed coat (Whelan 1995). Some tree species such
as Cupressus atlantica Gaussen (Youssef et al. 2012),
Elaeocarpus blascoi Weibel (Ramasubbu and Irudhyaraj
2016), Intsia bijuga (Colebr.) Kuntze (Thaman et al. 2006)
exhibit exogenous dormancy. In such species, water pen-
etration required for embryo growth and expansion is
inhibited by the hard seed coats. Mechanical dormancy
induced by seed coat impermeability is known to cause low
and erratic germination and is usually associated with the
presence of one or more layers of impermeable palisade
layers of lignified cells (Vazquez Yanes and Perez Garcia
1976; Corner 1976). The presence of galactomannan
polymers on the walls of the endosperm in the seeds of
Gymnocladus assamicus P.C.Kanjilal (Choudhury et al.
2009) has been attributed to its highly impermeable nature
(McCleary and Matheson 1974). Species with hard seed
coats can remain dormant for a period of few months as
 Author's personal copy
Ecology of seed germination in threatened trees: a review
observed in P. africana (Negash 2004) to as long as 5 years
as reported in C. atlantica (Youssef et al. 2012).
Endogenous dormancy is found in a number of plant
families such as Apiaceae, Aquifoliaceae, Araceae, Ara-
haceae, Aristolochiaceae, Berberidaceae, Fumariaceae,
Illiciaceae, Lardizabalanceae, Liliaceae, Magnoliaceae,
Papaveraceae, Ranunculaceae and Schisandraceae
(Grushvitzky 1967). There are insufficient studies in fam-
ilies with underdeveloped embryo, thus limiting the
knowledge of whether seeds have morphological or mor-
pho-physiological dormancy (Baskin and Baskin 1998).
Morphological dormancy has been documented in only two
temperate families, i.e. Apiaceae and Ranunculaceae
(Baskin and Baskin 1998). In the present review, most of
the species exhibited morpho-physiological dormancy
(MPD). Magnoliaceae members viz. M. punduana (Iralu
and Upadhaya 2016), M. schiedeana (Vásquez-Morales
and Sánchez-Velásquez 2011), M. ingrata (B.L.Chen &
S.C.Yang) Figlar (Han and Long 2010), Michelia yunna-
nensis (Hu) Noot. (Han et al. 2010), Manglietiastrum
sinicum Y.W. Law (Zheng and Sun 2009) and Magnolia
grandis (Hu & W.C.Cheng) V.S. Kumar (Pan and Sun
2009), have underdeveloped embryos at the time of mat-
uration indicating the presence of morpho-physiological
dormancy. In M. punduana, the embryos were small and
differentiated into cotyledons and radicle that continued to
grow inside the seeds after dispersal (Iralu and Upadhaya
2016). The seeds of M. dealbata have been thought to
exhibit exogenous dormancy caused by oils and inhibitors
of the sarcotesta and lignified testa (Vovides and Iglesias
1996). However, endogenous dormancy and natural ger-
mination after 9 months of seed dispersal were reported by
Corral-Aguirre and Sanchez-Velasquez (2006) in Mexico.
This revealed that seeds of M. dealbata are subjected to a
natural cold stratification when exposed to 10–20 days of
frost per year (Zulueta–Rodrı́guez and Soto 1993). Similar
results on natural stratification have been reported in M.
punduana (Iralu and Upadhaya 2016) whereby low tem-
peratures gradually release the nutrient reserves of the
endosperm for the growth of the embryo, allowing its
survival during winter (Camacho 1994).
The germination of seeds in Pritchardia remota
(Kuntze) Becc. (Perez et al. 2008) and Podocarpus
angustifolius Griseb. was delayed by 4 weeks due to MPD
induced by the presence of a lineal and rudimentary
underdeveloped embryo (Ferrandis et al. 2011), while, in I.
paraguariensis, MPD was attributed to the woody endo-
carp as whole pyrenes failed to germinate even after
120 days as opposed to bisected pyrenes that germinated
successfully (Almeida et al. 2000; Dolce et al. 2010). The
seeds of P. angustifolius needed an additional 9 days to
achieve a high value of germination suggesting the
195
existence of a physiological dormancy (Baskin and Baskin
1998).
A new type of dormancy in Humboldtia laurifolia M.
Vahl characterized by considerably delayed plumule (ca.
50 days) and radicle emergence (within 18 days) was
observed (Jayasuriya et al. 2010). The epicotyl elongated
very slowly with a length of * 15–17% of that of the seed
at the beginning of plumule growth which increased to
23–25% at the time of shoot emergence. The dormancy in
this species was attributed to the epicotyl and later classi-
fied as non-deep physiological dormancy of the plumule.
Though failure in seed germination is attributed to the
presence of either exogenous or endogenous seed dor-
mancy or both and is viewed as an obstacle in propagation,
it is in fact an adaptive strategy that ensures the survival of
the species through periods of environmental stress under
natural conditions.
2.5 Overcoming seed dormancy
Depending on the type of dormancy present in seeds,
various treatments have been applied for overcoming dor-
mancy. Some of the most common techniques used are
listed below:
1. Scarification, which can be of two types viz. mechan-
ical and chemical. In the former, the hard seed coat is
cracked open or subjected to physical abrasion whereas
in the latter, seeds are soaked in concentrated acid for
specific amount of time depending on the thickness of
the testa.
2. Stratification (seeds subjected to chilling)
3. Storage conditions (temperature, moisture and
substratum).
4. The application of gibberellins (GA3) can overrule
photodormancy, thermodormancy, dormancy imposed
by incomplete embryo development, mechanical bar-
riers and the presence of germination inhibitors
(Bewley and Black 1994).
A combination of treatments can also be used in
breaking dormancy. A brief review of each of the dor-
mancy-breaking techniques applied in most of the species
has been summarized as follows:
2.5.1 Scarification
Many species exhibit physical impediments to water per-
meability imposed by the presence of hard seed coat.
Species belonging to Leguminosae, Cannaceae, Mal-
vaceae, Convolvulaceae and Elaeocarpaceae are charac-
terized by an impermeable seed coat. The hard seed coat
may confer tolerance to heat (Whelan 1995). Under natural
conditions, fire plays a key role in regeneration where it
123
 Author's personal copy
196
cracks the seed coats and promotes germination (Baskin
and Baskin 1998) and induces the release of other chemical
components that are known to stimulate seed germination
(Van Staden et al. 2000; Hilhorst et al. 2006). Seeds of
Quercus robur L. when exposed for 10 and 15 min to
smoke and charcoal had a germination percentage of
90–94% (Reyes and Casal 2006). Seeds of S. macrophylla
had a cumulative germination of 13% after slash, fell and
burn treatment (Negreros-Castillo et al. 2003). Subjecting
seeds to varying periods of water submersion and tem-
peratures fluctuations can break dormancy in certain spe-
cies. Scarification of seeds by nicking a part of the seed
coat or by rubbing the seeds against a rough surface is
known to increase germination in many species. Germi-
nation percentage ([ 67%) in seeds of C. atlantica was
obtained upon hand scarification with sand paper (Youssef
et al. 2012). When soaked in water at a temperature of
60 °C and 80 °C for 15 min, seeds of this species germi-
nated to 34% and 67%, respectively, in comparison to the
control (18%). Nicked seeds of T. mucronatum placed on
moist filter paper showed germination of about 14% (Hi-
laire 2001). The seeds of Baikiaea plurijuga Harms showed
75% germination upon mechanical scarification, and 100%
germination upon hot water pre-soaking for 9 min, whereas
chemical scarification of the seeds in 98% H2SO4 for more
than 3 min drastically reduced germination percentage.
The seeds of this species have a weak seed coat and
required pre-soaking in hot water (Botsheleng et al. 2014).
Similarly, in G. assamicus mechanical scarification and hot
water treatment improved germination significantly by
65–80%, while untreated seeds showed 42% germination.
Chemical scarification of the seeds in concentrated H2SO4
for 40 min also increased the germination to [ 55%
(Choudhury et al. 2009).
A combination of hydropriming (sterile distilled water
with a constant supply of oxygen) and biopriming using
rhizobacteria Pseudomonas fluorescens and Bacillus sub-
tilis strain on the germination of two endangered fir Abies
hickelii Flous & Gaussen and A. religiosa resulted in 91%
and 68% germination, respectively (Zulueta-Rodrı́guez
et al. 2015). Similarly, in M. schiedeana, a combination of
mechanical scarification, cold stratification at 4–10 °C and
soaking in water of varying temperature improved seed
germination to 84% (Vásquez-Morales and Sánchez-
Velásquez 2011). On the other hand, manual scarification
reduced germination in M. punduana to 20% (Iralu and
Upadhaya 2016) whereas manual aril removal increased
the germination of Magnolia pugana (H.H. Iltis & Vaz-
quez) A. Vazquez & Carvajal to 52% (Jacobo-Pereira et al.
2016). Thus, physical dormancy imposed by the presence
of structural impediments can be overcome by various
exogenous factors such as fire that induces the release of
other chemical components known to stimulate seed
123
V. Iralu et al.
germination. Dormancy can also be broken by water sub-
mersion and temperatures fluctuations in certain species as
well as scarifying. However, various combinations of
mechanical scarification and hot water treatment (Baikiaea
plurijuga and G. assamicus); hydropriming and biopriming
(A. hickelii and A. religiosa) cold stratification (M. schie-
deana) and soaking in water of varying temperature (C.
atlantica) can significantly improve germination.
2.5.2 Stratification
Stratification of seeds to varying periods of chilling is
known to break dormancy especially in species exhibiting
MPD. Seeds of M. dealbata stratified in barren humid sand
exposed to a chilling temperature of 4–10 °C and sub-
merged for 24 h in room temperature (18–20 °C) yielded a
germination of 100% (Corral-Aguirre and Sanchez-Ve-
lasquez 2006). Cold stratified seeds of M. yunnanensis
germinated to 89% and 71% after 80 and 100 days of
stratification, respectively (Han et al. 2010). Similarly, cold
stratification for 90 days yielded high germination (93%)
in Magnolia punduana (Iralu and Upadhaya 2016),
whereas M. grandis attained highest germination after
60 days (Pan and Sun 2009). Seeds of Picea omorika
(Pancic) Purk. required a temperature of 4 °C for ca.
6 weeks for germination (Gosling 2007). However, in
some species cold stratification resulted in no germination.
Seeds of M. dactyloides stored at a low temperature
(0–5 °C) failed to germinate probably due to cell damage
or the formation of ice crystal within cells (Bewley and
Black 1994). Although cold stratification to varying peri-
ods of chilling is known to overcome dormancy, it may
also result in germination failure.
2.5.3 Light, temperature, and substratum
Extrinsic factors such as light, temperature and a growing
substratum may substantially affect seed germination and
seedling survival (Bargali et al. 1998; Everham et al.
1996). High germination in seeds of Jacaranda mimosifo-
lia D.Don was observed in both light and dark conditions at
a temperature of 25 °C (Socolowski and Takaki 2004).
Seeds of Picconia azorica (Tutin) Knobl., when stored at
low temperature (10/5 °C) followed by warm stratification,
germinated successfully, thus suggesting that warm tem-
perature contributes to embryo development (Martins et al.
2012). Seeds of M. dactyloides when stored in different
substratum for 3 months at 20 °C showed high germination
in germination paper (88%) in comparison to moist ver-
miculite, mineral soil, sand, sponge sheet and cotton towel
(Sivakumar et al. 2006). A pre-treatment of soaking seeds
in hot water for 15 min and thereafter sowing in a sub-
stratum of 1:2:1 mixture of garden soil, poultry dung and
 Author's personal copy
Ecology of seed germination in threatened trees: a review
sawdust resulted in 92% germination in Milicia excelsa
(Wele.) C.C. Berg. (Nzekwe et al. 2013). Bannister et al.
(2014) reported that moist substrates composed of sphag-
num or mineral soil were best suited for seed germination
of P. uviferum (ca. 60%). A combination of chemical
scarification in H2SO4 followed by culture on solid nutrient
medium resulted in a germination of 86–94% in Maytenus
canariensis (Loes.) G. Kunkel & Sunding (Gutiérrez-Ni-
colás et al. 2008). Padmalatha and Prasad (2007) reported
that under in vitro conditions, seeds of the endangered tree
Pterocarpus santilinus L.f. when soaked overnight in tap
water followed by mechanical scarification resulted in
100% germination on Murashige and Skoog-MS (liquid)
medium. Seeds of P. alba exhibited low germination per-
centages at low temperature (10/5 °C), whereas at high-
temperature regimes (20/10 °C, 25/15 °C and 35/20 °C),
seeds from all the provenances showed high germination
percentages (Venier et al. 2015). Similar observations were
made in Prosopis caldenia Burkart where a high temper-
ature applied for few minutes promoted seed germination
(de Villalobos et al. 2002). Alternating temperature of 20°
and 30 °C resulted in 65% germination in M. officinalis,
whereas a temperature of 20° and 10 °C was favourable for
M. grandis with 36% germination. A temperature of
22.3 °C was optimum for the germination of P. besseri and
fluctuating the temperature between 20/10 °C resulted in
93% germination (Gareca et al. 2012). Asomaning et al.
(2010) reported that the germination of Khaya anthotheca
(Welw.) C. DC. showed better response at 20 °C and 30 °C
and alternating the temperature regimes at 5/30 °C,
20/25 °C, 20/35 °C, 25/15 °C, 25/30 °C, 30/20 °C, and
5/15 °C resulted in 100% germination. Seeds of P. azorica
performed best under alternating temperatures of 10/5 °C
and 15/10 °C with a germination of 62% (Martins et al.
2012). Seeds of S. globulifera and Pterogyne nitens Tul.
showed better germination at higher temperatures
(20–35 °C) (Corbineau and Côme 1989; Morandini et al.
2013). Studies on the germination of Eriotheca vargasii
(Cuatrec.) A. Robyns (Malvaceae), an endemic Peruvian
Andean tree, revealed that substrate moisture levels had no
influence on germination capacity or rate. However, tem-
perature (25 °C) and substrate type (commercially pre-
pared media) showed strong effects on germination (90%)
(Mamani et al. 2018). Thus, one of the most effective
treatments for germination was incubation of seeds in
different temperature regimes as observed in 19 species.
Some species either responded to a constant temperature
treatment (P. besseri) or a fluctuating temperature regime
(P. alba, S. globulifera, Pterogyne nitens Tul., and M.
grandis), whereas others (P. remota, M.schiedeana)
exhibited successful seed germination on incubation in
combination with mechanical treatment.
197
In addition to soil temperature and moisture, seed ger-
mination is also affected by light intensity. Germination of
P. sylvetris under field conditions was highest (95%) in
shade-free microhabitats and high soil temperature (mean
max—21 °C), while germination was delayed under low
light intensity (Nyman 1963; Tillberg 1992). The optimum
temperature for Nyssa yunnanensis W.Q. Yin ex H.N. Qin
& Phengklai was 25 °C. The seeds germinated better in
light (12 h/day) than in dark treatment (Yuan et al. 2013).
The effect of different light intensity and soil moisture on
the seed germination of Parashorea chinensis Wang Hsie
revealed that 40% light and 60% soil moisture was opti-
mum for germination (Xiaojin 2015). However, seed ger-
mination and seedling establishment of M. patungensis,
under four soil types and three shade treatments (0%, 40%
and 80% of full sunlight) showed that germination rate was
low (19–31%) and soil type had no significant effect on
seed germination rate. Seedling survival and growth rate
increased with increasing light intensity and also promoted
biomass accumulation and root development. The seedling
survival rate was highest (91%) in the farmland soil but
reduced to 80%, 78% and 53% in old-field soil, sandy soil
and forest soil, respectively (Chen et al. 2012). In the
present study, seeds of nine species were positively pho-
toblastic and responded to light treatment. Thus, varying
periodicities and intensities of light condition, temperature
as well as a growing substratum affect seed germination in
many tree species.
2.5.4 Plant growth regulators
Plant hormones are known to regulate many physiological
and bio-chemical processes in plant. Some of the mecha-
nisms controlled by growth regulators include cell division,
growth and differentiation (Hooley 1994) and seed dor-
mancy and germination (Graeber et al. 2012). Abscisic acid
(ABA) inhibits cell cycle (Sanchez et al. 2005) and initiates
dormancy (Groot and Karssen 1992) and hence, ABA
deficient seeds exhibit rapid germination. Nitrates in plants
can act as a source of nitrogen as well as enhance seed
germination (Atia et al. 2009). Plant hormones like ethy-
lene and gibberellins affect radicle growth. Gibberellins are
the most important for the production of mannanase which
is necessary for seed germination (Wang et al. 2005) as it
stimulates the synthesis and production of the hydrolases,
especially a-amylase, resulting in seed germination (Ap-
pleford and Lenton 1997; Yamaguchi 2008) by inhibiting
ABA activity. Auxins (IAA) also play a key role in regu-
lating cell cycling, growth and development, formation of
vascular tissues (Davies 2013) and pollen (Ni et al. 2002)
and development of other plant parts (He et al. 2000).
External application of GA3 in M. sinicum showed a ger-
mination of 66% when the seeds were soaked for 24 h in
123
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198
500 mg L-1 GA3. Application of GA3 along with light was
useful in breaking dormancy in S. album (Das and Tah
2013; Vijayan and Rahees 2015). Seeds of M. yunnanensis
soaked in 2000 mg L-1 GA3 for 48 h germinated to 94% at
a temperature of 25 °C and 20/25 °C (Han et al. 2010).
Similarly, GA3 induced germination has been reported in
M. punduana where seeds soaked in 3000 mg L-1 GA3 and
incubated at 25 °C germinated to 77% (Iralu and Upadhaya
2016). Similarly, mechanically split seeds of Elaeocarpus
prunifolius Wall. Ex Müll. Berol. treated with GA3
(3000 mg L-1) yielded a germination of 24% (Iralu and
Upadhaya 2018). GA3 induced faster germination in C.
atlantica at 1000 and 2000 mg L-1 (Youssef et al. 2012).
Sivakumar et al. (2006) reported that application of
1000 ppm GA3 (ca. 63.5%) as well as 1000 ppm IBA
(94.5%) initiated germination of M. dactyloides seeds
stored at 15 or 20 °C for 3 months. The comparatively
significant effect of indoleacetic acid (IAA) than naph-
thylacetic acid (NAA) on the seed germination of Jacar-
anda mimosifolia D. Don when kept in an illumination
incubator at 25 °C/18 °C under 15 h light was reported by
Zhou et al. (2012). The seeds of endangered tree Mansonia
altissima (A.Chev) A.Chev. when soaked in 0.02 g L-1
IAA for 24 h and sown in a substratum of washed river
sand showed a germination of 66% and 0.01 g L-1 and
0.03 g L-1 IAA had a germination of 62%. Indole-3-bu-
tyric acid (IBA) treatment of 0.02 g L-1 also yielded 62%
germination but low concentration reduced germination to
38% (Maku et al. 2014). The application of nitrate (KNO3)
did not promote germination of M. yunnanensis (Han et al.
2010) and E. prunifolius (Iralu and Upadhaya 2018) seeds.
Similarly, seeds treated solely with KNO3 resulted in low
germination (16%) in M. punduana (Iralu and Upadhaya
2016) and 2% in P. santilinus (Padmalatha and Prasad
2007). A combination treatment of GA3 and alternating
temperature (10–40 °C) improved germination of Ptero-
carpus angolensis DC (van Daalen 1991). In B. ovalifoli-
olata, application of silver nanoparticles (SNPs) had a
significant effect on germination. Seeds planted in MS
medium with different concentration of SNPs exhib-
ited [ 90% germination with the highest in 30 lg ml-1
(Savithramma et al. 2012). The high germination has been
attributed to the penetrating property of SNPs into the seed
coats resulting in embryo activation. The dormancy in Si-
nojackia xylocarpa Hu was broken by a combination
treatment of H2SO4, 500 mg L-1 GA3 and cold stratifica-
tion (Xiaohua et al. 1999). Similarly, in Leitneria floridana
Chapman, a treatment of various combinations such as
removal of fleshy endocarp and subsequent treatment in
GA3, leached drupes treated with GA3, seeds scarified in
96% H2SO4, treated in GA3 and chilling improved ger-
mination (Sharma and Graves 2004). Thus, plant growth
regulators play a key role in enhancing seed germination.
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V. Iralu et al.
The use of PGRs (GA3, IAA, IBA SNPs etc.) and cold
stratification in combination with an incubation treatment
was found to be effective for breaking dormancy and
enhancing germination in many species (M. sinicum, M.
yunnanensis and M. punduana). However, the selection of
the combination of various growth hormones, substratum
and growth conditions needs to be evaluated that may vary
with seed type.
3 Conclusion
The present investigation revealed that the major threats to
the decline of threatened species is attributed but not
confined to extraction of timber and Non-Forest Timber
Products (NTFPs) with a concomitant poor natural regen-
eration. Other factors such as habitat degradation, poor
regeneration and low population also contributed in part to
the decline of the species. The formation of seed banks in
the soil can be viewed as a strategy for species persistence
in nature especially for those with low natural population.
Majority of the species exhibited orthodox seeds and
required a pre-treatment for germination. Temperature
played a major role as an effective treatment for initiating
germination in many of the species. Furthermore, the use of
PGRs (GA3, IAA, IBA SNPs, etc.) and cold stratification in
combination with an incubation treatment was found to be
effective for breaking dormancy and improving germina-
tion. However, the present review revealed that there is
limited literature on the germination requirements of many
of the threatened species indicating lacunae in the field of
germination ecology. The findings highlight and emphasize
the need for detailed knowledge of seed structures and
factors affecting the growth potential of the embryo to
enable development of dormancy-breaking techniques. In
addition, methods of seed handling, storage behaviour and
germination of many threatened species are emphasized to
prevent extinction risks. Development of guidelines for
ecosystem management via seed germination protocols
will help maintain biodiversity values in ecological sys-
tems and aid the conservation of threatened species.
Compliance with ethical standards
Conflict of interest All authors declare that they have no conflict of
interest.
Appendix
See Table 1.
 Table 1 Seed type, germination treatments required and seed viability of threatened species
Species/family Forest type Reasons for decline IUCN Breeding Fruit Dispersal Seed Germination Seed viability References
status system type syndrome type treatments required (day/months)

Abies hickelii Tropical Deforestation, EN Monoecious Cone Anemochory ND Hydropriming and ND Zulueta-Rodrı́guez
Pinaceae logging biopriming et al. (2015)
Abies religiosa Tropical Timber LC Monoecious Cone Anemochory ND Hydropriming and ND Zulueta-Rodrı́guez
Pinaceae biopriming et al. (2015)
Alstonia Tropical ND LC Dioecious Follicle Anemochory ND Studied under natural ND Raich and Khoon
macrophylla conditions (1990)
Apocynaceae
Aquilaria Tropical Over-exploitation VU Cosexual Capsule Ballochory/ R No treatments required 15 days Tabin and Shrivastava
malaccensis for Agar, insect Anemochory (2014)
Aquilariaceae attacks
Baikiaea plurijuga Tropical Wildfires, habitat LR/ Cosexual Pods Ballochory ND Mechanical and acid ND Botsheleng et al.
Fabaceae change and NT scarification, hot (2014)
climate change water treatment
Boswellia Tropical Medicinal VU Cosexual Capsule Anemochory R Treatment with silver 15 days Savithramma et al.
Ecology of seed germination in threatened trees: a review

ovalifoliolata properties, low nanoparticles (2012)

Burseraceae germination,
slow growth
Canarium littorale Tropical ND LR/ Dioecious Nut Zoochory ND Studied under natural ND Raich and Khoon
Burseraceae LC conditions (1990)
Cupressus Temperate Habitat EN Monoecious Cone Anemochory O Hot water treatment, Ca 5 years Youssef et al. (2012)
atlantica degradation, mechanical
Cupressaceae overgrazing, poor scarification and
seed germination gibberellins
Dipterocarpus Tropical Harvesting of CR Cosexual Nut Anemochory ND Studied under natural ND Raich and Khoon
grandiflorus keruing timber conditions (1990)
Author's personal copy

Dipterocarpaceae and oleo-resin.

Elaeocarpus Tropical Low seed EN Cosexual Drupe Zoochory O ND ND Ramasubbu and
blascoi germination, Irudhyaraj (2016)
Elaeocarpaceae expansion of
agricultural
lands,
monoculture of
exotic tree
species
Elaeocarpus Subtropical Habitat VU Cosexual Drupe Zoochory O ND Ca 2 years Iralu and Upadhaya
prunifolius degradation (2018)
Elaeocarpaceae
Eriotheca vargasii Seasonally dry EN Cosexual Capsule Anemochory ND ND ND Mamani et al. (2018)
Malvaceae
199

123
 Table 1 continued
200

Species/family Forest type Reasons for decline IUCN Breeding Fruit Dispersal Seed Germination Seed viability References
status system type syndrome type treatments required (day/months)

123
Gymnacranthera Tropical Low population VU Dioecious Drupe Zoochory R No treatments required ca 2 months Keshavachandra and
canarica exclusively Krishnakumar
Myristicaceae restricted to (2016)
swamp areas
Gymnocladus Tropical Pods edible and CR Dioecious Pods Autochory O Mechanical 1 year Choudhury et al.
assamicus used for religious scarification and hot (2009)
Fabaceae purposes, poor water treatment
regeneration
Hopea odorata Tropical ND VU Cosexual Nut Anemochory R Shaded light ca 4 months Krishnapillay et al.
Dipterocarpaceae (1991)
Horsfieldia Tropical Seeds exploited for EN Cosexual Capsule Anemochory/ R 30 °C incubation, 10% ND Yu et al. (2008)
pandurifolia oil, tree yield Zoochory light
Myristicaceae good timber
Humboldtia Tropical Habitat VU Cosexual Pods NA R No treatments required 15 days Jayasuriya et al.
laurifolia degradation, (2010)
Fabaceae restricted
distribution
Hyophorbe Tropical Regeneration is CR Monoecious Nut NA R Dried seeds, higher ND Wood and Pritchard
lagenicaulis sporadic, light intensity (2003)
Arecaceae restricted
distribution
Ilex paraguariensis Tropical and Leaves used to LR/ Dioecious Drupe Barochory ND Nutrient media and ND Dolce et al. (2010)
Aquifoliaceae Subtropical make stimulant NT cold stratification and Almeida et al.
drink (2000)
Illicium griffithii Subtropical and Harvested for EN Cosexual Follicle Autochory ND Substratum of forest ND Mukhia (2006)
Schisandraceae temperate seeds, fruits and top soil ? litter
Author's personal copy

timber ash ? sand, open

areas of forest
Intsia bijuga Tropical Valuable timber in VU Monoecious Pods Autochory O Manual scarification 3 years Thaman et al. (2006)
Fabaceae South East Asia
Jacaranda Subtropical Agricultural VU Monoecious Capsule Anemochory ND Temperature and light ND Socolowski and
mimosofolia expansion Takaki (2004)
Bignoniaceae
Khaya anthotheca Tropical Over-exploitation VU Cosexual Capsule Anemochory ND Alternating ND Asomaning et al.
Meliaceae for timber, poor temperatures (2010)
regeneration and
genetic erosion
V. Iralu et al.
 Table 1 continued
Species/family Forest type Reasons for decline IUCN Breeding Fruit Dispersal Seed Germination Seed viability References
status system type syndrome type treatments required (day/months)

Leitneria floridana Riverine ND LR/ Dioecious Drupe Zoochory ND Treated in GA3, ND Sharma and Graves
Simaroubaceae NT scarification in 96% (2004)
H2SO4 and 24 h in
GA3 and cold
stratification, excised
fruits in GA3
Litsea pierrei Tropical Timber value, EN Dioecious Berry NA ND Intermediate shade ND Yu et al. (2008)
Lauraceae perfumes, low
population
Lophopetalum Tropical Exploited for LR/ Dioecious Capsule Anemochory R Sand bed 20–30 days Keshavachandra et al.
wightianum perupok timber LC (2014)
Celastraceae
Lysiloma Tropical dry ND LC Cosexual Pods Autochory O ND Ca 2 years Cervantes and Bonfil
acapulcense (2014)
Ecology of seed germination in threatened trees: a review

Fabaceae
Magnolia dealbata Cloud forest Habitat NT Dioecious Follicle Zoochory SR Warm and cold 1 year Corral-Aguirre and
Magnoliaceae degradation, stratification, Sanchez-Velasquez
limited temperature (2006)
distribution
Magnolia ingrata Subtropical ND DD Dioecious Follicle Zoochory R Cold stratification and ND Han and Long (2010)
Magnoliaceae GA3
Magnolia Tropical Bark of medicinal EN Cosexual Follicle Zoochory SR Differential ND Shu et al. (2010)
officinalis value, seed set temperature, light,
Magnoliaceae and germination soil water content,
low water treatment
Magnolia pugana Tropical Deforestation, EN Cosexual Follicle Zoochory ND Manual aril removal ND Jacobo-Pereira et al.
Author's personal copy

Magnoliaceae habitat (2016)

degradation
Magnolia Tropical Exploited for DD Cosexual Follicle Zoochory SR Plant growth hormones 1 year ca when Iralu and Upadhaya
punduana timber, habitat (GA3), Cold stored at 5 °C (2016)
Magnoliaceae destruction stratification, in moist sand
temperature substrate
Magnolia Tropical Restricted VU Cosexual Follicle Zoochory O Combination of Ca 2 years Vásquez-Morales and
schiedeana distribution, mechanical Sánchez-Velásquez
Magnoliaceae habitat scarification, (2011)
destruction, low stratification and
seed production warm water
treatment
Magnolia Subtropical and ND DD Cosexual Follicle Zoochory SR Plant growth hormones ND Han et al. (2010)
yunnanensis Temperate (GA3), Cold
Magnoliaceae stratification,
temperature
201

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 Table 1 continued
202

Species/family Forest type Reasons for decline IUCN Breeding Fruit Dispersal Seed Germination Seed viability References
status system type syndrome type treatments required (day/months)

123
Manglietia grandis Tropical and Habitat loss, CR Cosexual Follicle Zoochory SR Alternating ND Pan and Sun (2009)
Magnoliaceae Subtropical economically temperatures, cold
important trees stratification and
GA3
Manglietia Tropical Lack of natural EN Dioecious Follicle Zoochory ND Fruits stored in moist ND Chen et al. (2012)
patungensis regeneration, sand at 4 °C in dark
Magnoliaceae fragmentation, to break dormancy
over-exploitation
Manglietiastrum Subtropical Exploited for CR Cosexual Follicle Zoochory SR Plant growth hormones ND Zheng and Sun (2009)
sinicum timber, habitat (GA3), Cold
Magnoliaceae destruction stratification,
temperature
Mansonia altissima Tropical Exploited for EN Monoecious Nut Anemochory ND Indole acetic acid, ND Maku et al. (2014)
Malvaceae timber Indole 3-butyric acid
Maytenus Thermophilous Decline in forest VU Cosexual Capsule Zoochory ND H2SO4 ? surface ND Gutiérrez-Nicolás
canariensis forest area strerilization and et al. (2008)
Celastraceae culture on solid
nutrient medium.
Milicia excelsa Tropical Timber LR/ Dioecious Syncarp NA ND washing in water and ND Nzekwe et al. (2013)
Moraceae exploitation NT soaking for 15 min
in hot water (50 °C)
Myristica Tropical Harvested for VU Dioecious Drupe Zoochory SR GA3 at 15 °C and IBA up to 3 months at Sivakumar et al.
dactyloides fruits, medicine, at 20 °C 20 °C (2006)
Myristicaceae habitat loss
Myristica Tropical Conversion of VU Dioecious Drupe Zoochory R No treatments required 1 week Kumar et al. (2002)
malabarica swamp areas to
Author's personal copy

Myristicaceae agricultural land

Nothocestrum Tropical ND EN Cosexual Drupe Autochory R No treatments required ND http://www.cpp.edu/
breviflorum *ejquestad/
Solanaceae hawaiipropguide/
Nothocestrum%
20breviflorum.html
Nothofagus glauca Temperate Habitat converted VU Monoecious Nut Zoochory R ND ND Burgos et al. (2008)
Nothofagaceae into Pinus
radiata
plantation
Nyssa yunnanensis Tropical Logging CR Dioecious Drupe NA O Temperature, GA3 and ND Yuan et al. (2013)
Nyssaceae light
Olearia hectorii Tropical Germination and DD Cosexual Achene Anemochory ND Light required for ND Rogers (1996)
Asteraceae seedling growth germination
failure
V. Iralu et al.
 Table 1 continued
Species/family Forest type Reasons for decline IUCN Breeding Fruit Dispersal Seed Germination Seed viability References
status system type syndrome type treatments required (day/months)

Parashorea Tropical Insect attacks, EN Cosexual Nut Anemochory ND Moisture and light ND Xiaojin (2015)
chinensis over-exploitation
Dipterocarpaceae for timber
Phoebe bournei Tropical and Timber LR/ Cosexual Drupe Zoochory R No treatments required ca 3 months Darong and Bosun
Lauraceae Subtropical NT (2001)
Picconia azorica Tropical Over-exploitation EN Cosexual Drupe Zoochory O Acid scarification, ND Martins et al. (2012)
Oleaceae of the wood, removal of endocarp,
habitat loss cold stratification,
alternating
temperature
Picea omorika Subtropical Fire, low EN Monoecious Cone Anemochory O Cold stratification ND Gosling (2007)
Pinaceae regeneration
Pilgerodendron Temperate Over-exploited for VU Dioecious Cone Anemochory O A substrate of moss, Up to 5 months Bannister et al. (2014)
uviferum constructions, mineral soil
Ecology of seed germination in threatened trees: a review

Cupressaceae fragmentation
and isolation.
Pinus sylvestris Tropical Short germination LC Monoecious Cone Anemochory R Studied under natural ND Castro et al. (2005)
Pinaceae period, seed conditions
predation
Podocarpus Tropical Fire, mining VU Dioecious Drupe Autochory/ SR ND ND Ferrandis et al. (2011)
angustifolius Zoochory
Podocarpaceae
Poeciloneuron Tropical and Timber extraction, CR Dioecious Capsule NA R No treatments required ND Koilpillai (2017)
pauciflorum Subtropical habitat loss
Clusiaceae
Author's personal copy

Polylepis besseri Tropical Burning, over VU Cosexual Winged Anemochory O Temperature of 22 °C ND Gareca et al. (2012)
Rosaceae grazing, soil fruit
erosion and
firewood
collection
Pritchardia remota Scrub Feral animal EN Monoecious Nut Zoochory O Endocarp removal and ND Pérez et al. (2008)
Arecaceae attacks incubation at
25–35 °C
Prosopis alba Semi-arid Exploited for LR/ Cosexual Pods NA O Alternating ND Venier et al. (2015)
Fabaceae timber NT temperature above
10–35 °C
Prosopis caldenia Semi-arid Food and fuel DD Cosexual Pods NA O High temperature for ND de Villalobos et al.
Fabaceae few minutes (2002)
Prunus africana Tropical Timber and VU Cosexual Drupe Zoochory R Soil and decomposing ca 2 months Negash (2004)
Rosaceae medicine litter, GA3
extraction
203

123
 Table 1 continued
204

Species/family Forest type Reasons for decline IUCN Breeding Fruit Dispersal Seed Germination Seed viability References
status system type syndrome type treatments required (day/months)

123
Pterocarpus Tropical Overexploitation, LR/ Cosexual Pods Autochory R Moderate levels of fire 30 days van Daalen (1991)
angolensis attack by fungi, NT to stimulate
Fabaceae poor regeneration germination; GA3
with alternating
temperatures
Pterocarpus Tropical Valuable timber, EN Cosexual Pods Autochory R Murashige and Skoog ND Padmalatha and
santalinus extraction of dye, media with 3% Prasad (2007)
Fabaceae medicine and sucrose
cosmetics
Pterogyne nitens Tropical dry Logging, LR/ Cosexual Achene Anemochory ND Temperature range of ND Morandini et al.
Fabaceae encroaching NT 24–30 °C (2013)
agriculture and
pastoralism
Quercus robur Tropical ND LC Monoecious Nut Zoochory R 1 year incubation at ND Reyes and Casal
Fagaceae 4 °C followed by: (2006)
smoke–10–15 min,
and charcoal
treatment
Santalum album Tropical Wood used for VU Cosexual Drupe Zoochory O Full light and GA3 Ca 2 years Vijayan and Rahees
Santalaceae furniture, oils (2015) and Das and
used in cosmetics Tah (2013)
Santalum Subalpine ND VU Cosexual Drupe Zoochory O ND Ca 5 years Hirano (1990)
haleakalae
Santalaceae
Sapindus Tropical Seeds used as VU Dioecious Berry Zoochory ND Stratification ? moist ND http://tropical.
oahuensis laxative vermicullite, theferns.info/
Author's personal copy

Sapindaceae removal of seed coat viewtropical.

and bury at a depth php?id=
of 10–20 mm in soil Sapindus?oahuensis
Saraca asoca Tropical Over-exploitation VU Cosexual Pods NA R No treatments required \ 30 days Singh et al. (2005)
Fabaceae for
pharmaceutical
properties
Shorea multiflora Tropical ND LR/ Cosexual Nut Anemochory ND Studied under natural ND Raich and Khoon
Dipterocarpaceae LC conditions (1990)
Shorea trapezifolia Tropical Natural habitats CR Cosexual Nut Anemochory R Removal of seed 2 weeks de Zoysa and Ashton
Dipterocarpaceae converted to wings, partial shade (1991)
plantations, wood
used for making
plywood
V. Iralu et al.
 Table 1 continued
Species/family Forest type Reasons for decline IUCN Breeding Fruit Dispersal Seed Germination Seed viability References
status system type syndrome type treatments required (day/months)

Sinojackia Tropical Used as firewood VU Cosexual Drupe NA O Combination of acid ND Xiaohua et al. (1999)
xylocarpa scarification, GA3
Styracaceae and cold
stratification
Swietenia Tropical and Most important VU Monoecious Capsule Anemochory R 80% light ND Negreros-Castillo
macrophylla Temperate commercial et al. (2003)
Meliaceae mahagony, poor
regeneration
Swietenia Tropical Timber value, high EN Dioecious Capsule Anemochory SR No treatments required Cold storage at Schmidt and Jøker
mahagoni genetic erosion 2–5 °C with (2000)
Meliaceae 4–5% moisture
content extends
viability up to
1 year
Ecology of seed germination in threatened trees: a review

Symphonia Tropical and Medicinal property DD Monoecious Berry Zoochory R Temperature between Up to 3 years Corbineau and Côme
globulifera Subtropical 20 and 35 °C when stored at (1989)
Clusiaceae 15 °C
Taiwania Temperate Timber value VU Monoecious Cone Anemochory O ND ND http://www.
cryptomerioides dendrology.org/
Cupressaceae publications/tree-of-
the-year/taiwania-
cryptomerioides-
(2010)/
Talbotiella gentii Tropical dry Low population, CR Cosexual Pods Ballochory ND ND ND Dompreh et al. (2015)
Fabaceae charcoal and fuel
wood
Author's personal copy

Taxodium Riparian Timber value LC Monoecious Cone Anemochory ND Mechanical ND Hilaire (2001)
mucronatum scarification
Cupressaceae
Ternstroemia Tropical Habitat loss VU Dioecious Berry Zoochory ND Studied under natural ND Raich and Khoon
wallichiana conditions (1990)
Pentaphylacaceae
Vatica nitens Tropical Habitat loss EN Cosexual Nut Anemochory ND Studied under natural ND Raich and Khoon
Dipterocarpaceae conditions (1990)
IUCN The International Union for Conservation of Nature, CR critically endangered, EN endangered, VU vulnerable, NT near threatened, LC least concern, DD data deficient, O orthodox seeds,
R recalcitrant seeds, SR semi-recalcitrant, ND not documented
205

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