Vous êtes sur la page 1sur 24

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
Your article is protected by copyright and
all rights are held exclusively by The Joint
Center on Global Change and Earth System
Science of the University of Maryland and
Beijing Normal University. This e-offprint is
for personal use only and shall not be self-
archived in electronic repositories. If you wish
to self-archive your article, please use the
accepted manuscript version for posting on
your own website. You may further deposit
the accepted manuscript version in any
repository, provided it is only made publicly
available 12 months after official publication
or later and provided acknowledgement is
given to the original source of publication
and a link is inserted to the published article
on Springer's website. The link must be
accompanied by the following text: "The final
publication is available at link.springer.com”.

1 23
Author's personal copy
Energ. Ecol. Environ. (2019) 4(4):189–210


Ecology of seed germination in threatened trees: a review

Viheno Iralu1 • Humayun Samir Ahmed Barbhuyan2 • Krishna Upadhaya3

Department of Environmental Studies, School of Human and Environmental Sciences, North-Eastern Hill University, Shillong 793 022, India
Department of Botany, School of Life Sciences, North-Eastern Hill University, Shillong 793 022, India
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 Keywords Disturbance  Dormancy  Growth regulators 
the rapid decline of the world’s forests, over-exploitation Scarification  Treatments
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 1 Introduction
the presence of thick seed coat as well as physiological
factors such as seed dormancy. Studies pertaining to seed Trees constitute one of the most valuable components of
germination, storage behaviour, dormancy-breaking tech- the world’s biodiversity. They have ecological, cultural and
niques, particularly of threatened tree species at global economic values and are vital to the well-being of people
level are limited. Therefore, the present study was con- all around the world (Oldfield et al. 1998). Estimates of
ducted to assess the progress made in the field of seed global tree species richness range from 60,000 (Grandtner
germination as well as the challenges that exist in the 2005) to 100,000 taxa (Oldfield et al. 1998), approximating
regeneration of such species that are of conservation value. to about 15–25% of the 350,000–450,000 vascular plants of
The results obtained from the analysis of 78 threatened tree the world (Scotland and Wortley 2004; Petit and Hampe
species showed that moisture is a critical factor for recal- 2006). However, since the dawn of human settlement,
citrant seeds, while species with orthodox seeds require a many species have been subjected to various pressures
pre-treatment for breaking dormancy. Although most of the (Atkinson and Cameron 1993) not only because of global
studies on dormancy-breaking techniques have demon- climate change and land-use intensification, but also due to
strated the effectiveness of one or two methods on seed an increase in biosecurity challenges (Meurk and Hall
germination, a combination of treatments as well as use of 2006). Anthropogenic activities have brought about 10% of
plant growth regulators improved the ability of seeds to the world’s tree species close to the brink of extinction
germinate. Water, light, nutrients and a favourable sub- (Oldfield et al. 1998). According to the Intergovernmental
stratum are major regulatory factors that affect germina- Panel on Climate Change (IPCC), roughly 20–30 percent
tion, growth and establishment of tree species. The findings of vascular plants and higher animals on the globe are at
emphasize the need to develop guidelines for proper seed the risk of extinction as temperatures increase by 2–3 °C
handling and understand germination protocols necessary (Parry et al. 2007). It is very likely that even modest losses
for ecosystem management that would aid both in main- in biodiversity would cause consequential changes in
taining biodiversity values and conservation of threatened ecosystem services (Parry et al. 2007; Seppälä et al. 2009).
species. 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
& Krishna Upadhaya
upkri@yahoo.com rare and threatened species such as Gymnacranthera

Author's personal copy
190 V. Iralu et al.

canarica (King) Warb. (Keshavachandra and Krishnaku- about their ecology such as patterns of dispersion, germi-
mar 2016), Hyophorbe lagenicaulis (L.H.Bailey) nation and establishment are scattered. The present paper
H.E.Moore (Wood and Pritchard 2003), Magnolia dealbata brings together the information on the germination studies
Zucc. (Corral-Aguirre and Sanchez-Velasquez 2006) and with special reference to globally threatened trees. Trees
Magnolia schiedeana Schltl. (Vásquez-Morales and Sán- that fall under the various threat categories of the IUCN
chez-Velásquez 2011) have restricted distribution and low Red list (IUCN 2016) and ‘the world list of threatened
populations size and are, therefore, at a high risk of trees’ (Oldfield et al. 1998) were considered. The objective
extinction. The species that are represented by small pop- of the study was to evaluate whether sufficient efforts have
ulations and poor adaptability thus warrants prioritization been put forth for recovery of such species worldwide in
as major categories in biodiversity conservation (Paal order to prevent them from extinction in nature through
1998). In this regard, the Convention on International seed germination. Seed storage behaviour, dormancy-
Trade in Endangered Species of Wild Fauna and Flora breaking techniques and factors responsible for the decline
(CITES) Timber Working Group (TWO) was formed at the of germination of such threatened trees have also been
ninth Conference of the Parties (COP) for sustainable reviewed.
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 2 Results and discussion
assessed and established the impact of industrialization on
the loss of vegetation and forest degradation (Ahmed 2008; The present review includes a total of 78 species belonging
Yildirim et al. 2009). Oldfield et al. (1998) listed 7388 tree to 64 genera and 33 families. These include 69 angios-
species that have been evaluated as globally threatened. perms belonging to 56 genera and 30 families. There were
Propagation of trees most commonly occurs through nine gymnosperms belonging to eight genera and three
seeds as they are the carriers of genetic resources for families. Fabaceae with 12 species and Magnoliaceae (10
species biodiversity, ecosystem restoration, conservation species) were the dominant families followed by Diptero-
and domestication (Berjak and Pammenter 2004). As a carpacea (6 species) and Cupressaceae (4 species). Of these
result, in recent years, seed germination studies have nine species are categorized as critically endangered, 19 as
emerged as an important tool for conservation of species. endangered and 26 vulnerable (‘‘Appendix’’ section).
Seed germination studies help in understanding the causes Twenty-eight species including Abies religiosa (Kunth)
of species decline, persistence or spread in changing Schltdl. & Cham., Dipterocarpus grandiflorus (Blanco)
landscapes (Schütz 2000). However, seed germination in Blanco, Horsfieldia pandurifolia H. H. Hu, Magnolia
many threatened trees is convoluted due to seed dormancy. punduana (Hook. f. & Thomson) Figlar, Pilgerodendron
In addition, viability and storage requirements of seed in uviferum (D. Don) Florin, Prosopis alba Griseb., Prunus
many species are unknown, making it difficult for ex situ africana (Hook.f.) Kalkman, Swietenia macrophylla King,
germplasm conservation. The knowledge on the germina- Taxodium mucronatum Ten. were on the decline due to
tion, storage behaviour and ecological requirements of rampant timber extraction and seven species including
many of the threatened trees remains unexplored and is a Boswellia ovalifoliolata N. P. Balakr. & A. N. Henry, H.
prerequisite for any conservation initiatives. pandurifolia, Ilex paraguariensis A. St.-Hil., Illicium
Seed production, dispersion, predation and germination griffithii Hook. f. & Thomson, Magnolia officinalis Rehder
are ecological processes, which affect the maintenance of & E. H. Wilson, Myristica dactyloides Gaertn., Saraca
the populations and their colonization in space and time asoca (Roxb.) Willd., Sapindus oahuensis Hillebr. ex
(Alexander et al. 2001; Baskin and Baskin 1998; Lorente- Radlk., Symphonia globulifera L. f., were subjected to
Adame and Sánchez-Velásquez 1996). Fragmentation and over-extraction as non-timber forest products (NTFPs) in
habitat loss have adverse effects on these processes. the form of leaves, fruits, seeds, etc., owing to their
However, the effects of forest fragmentation on pre-dis- medicinal properties, thus hindering their natural regener-
persal seed predation have been poorly addressed in trop- ation. Species such as P. africana and Pterocarpus san-
ical and subtropical forests (Cascante et al. 2002; Chacoff talinus L.f. are highly exploited for timber as well as their
and Aizen 2006). It is evident that there is low abundance, medicinal value (‘‘Appendix’’ section).
diversity and species richness of seed predators in small The distribution of the 78 tree species considered in the
fragments due to environmental fluctuations (Didham present study revealed that 63 species were tropical, 13
1997; Baguette and Schtickzelle 2003; Chacoff and Aizen subtropical and 6 temperate. Riparian, riverine, scrub and
2006). subalpine were poorly represented in the list with one
Although a number of studies on seed germination are species each (‘‘Appendix’’ section). Region-/country-wise
available from different parts of the world, information distribution of the species showed that India (17 species)

Author's personal copy
Ecology of seed germination in threatened trees: a review 191

and China (14 species), the two most populated countries also generate only male (‘‘andro’’) or female (‘‘gyno’’)
of the world, top the list followed by South America (11 functional parts, but not both. In addition, any tree might
species), Africa (10 species), Mexico (9 species) and produce only cosexual, male, or female flowers, in any
Malaysia and USA (6 species each). The rest of the 12 combination (Coder 2008). Of the 78 species reviewed in
countries had either one or two species each (Fig. 1). the present study, cosexuality was exhibited exclusively by
However, in the present analysis, countries like Australia, angiosperms (41species), a vast majority of which belon-
Philippines and Indonesia were poorly represented (‘‘Ap- ged to Fabaceae (10 species) followed by Magnoliaceae (7
pendix’’ section). A critical analysis of the threats operating species) and Dipterocarpaceae (6 species), while dioecy
on the species considered in the present paper revealed that was exhibited by 19 angiosperms and 2 gymnosperms and
timber extraction, habitat degradation, poor regeneration, monoecy was present in 9 angiosperms and 7 gym-
low population and land-use change were the major threats nosperms. Dioecious species grow more slowly than
responsible for the decline of these species (‘‘Appendix’’ cosexual taxa as they are unable to self-pollinate and
section). require another individual for seed production (Schlessman
et al. 2014; Xia et al. 2013; Öster and Eriksson 2007). For
2.1 Sexual reproduction and fruit type such plants, pollinator plays an important role in seed
production (Vamosi et al. 2006). The flowers of Olearia
Sexual reproduction and seed set in species are affected by hectorii Hook. f. are mostly perfect, i.e. have functional
dicliny either monoecy or dioecy. A single tree could have male and female elements, and are probably insect-polli-
flowers with both fully functional male and female parts nated. Light partly controls reproductive vigour, because
(cosexual, bisexual, perfect, or hermaphroditic) or could shaded limbs and trees produce few flowers, whereas full

Fig. 1 Number of species in

different regions/countries
considered in the present study

Author's personal copy
192 V. Iralu et al.

light initiates abundant flowering (Rogers 1996). However, types (Thompson and Grime 1979; Thompson et al. 1997).
43% of angiosperm families have dioecious members A persistent seed bank ensures the conservation of a spe-
(Renner 2014; Renner and Ricklefs 1995), prevalent cies as a fraction of seeds remains viable in the soil until
mostly in tropical or island flora as compared to the global the next seed dispersal event, thus contributing to the
proportion of 6% (Queenborough et al. 2009; Vary et al. resilience of plant populations even when no seeds are
2011). The taxonomical and geographical ubiquity of produced in a given year (Baskin and Baskin 1978; Baker
dioecious species suggests that they compensate for their 1989). This can even facilitate re-colonization after a local
reproductive disadvantages through ecological traits that extinction (Milberg 1994). Although many threatened trees
allow them to coexist with cosexual competitors. On the exhibit recalcitrant seed behaviour, they do not form per-
other hand, monoecious trees separate genders into dif- sistent seed banks as observed in Pinus sylvestris L. (Castro
ferent flowers within the same individual tree to minimize et al. 2005), whereas certain other species such as M.
selfing. Wind-dispersed seeds and temperate zone climates dealbata, M. schiedeana, M. punduana and Podocarpus
are associated with monoecy (Ohya et al. 2017). angustifolius Griseb. can form persistent seed banks in the
In terms of fruit type, dioecious trees have large, fleshy, soil (Corral-Aguirre and Sanchez-Velasquez 2006; Vás-
single-seeded fruits that are dispesed by animals, as evident quez-Morales and Sánchez-Velásquez 2011; Iralu and
by the presence of 10 dioecious and nine cosexual species Upadhaya 2016; Ferrandis et al. 2011). Buried seeds of M.
exhibiting drupe/berry fruits (‘‘Appendix’’ section). How- dealbata remained viable for 1 year (Corral-Aguirre and
ever, monoecious trees tend to exhibit cone type fruit as Sanchez-Velasquez 2006) and that of M. schiedeana for
observed in seven species. Fruit dispersal syndromes of the 2 years (Vásquez-Morales and Sánchez-Velásquez 2011).
studied species showed that majority were zoochorous (29 The persistence and viability of M. dealbata seeds was
species) and 17 species were anemochorous. In gym- however, limited by the availability of moisture (Corral-
nosperms, anemochory was the major dispersal syndrome Aguirre and Sanchez-Velasquez 2006) as also reported in
(8 species). M. punduana (Iralu and Upadhaya 2016). Formation of
seed banks is essential for maintaining population viability.
2.2 Seed set and seed banks Therefore, even in the case of lower seed production in a
given year as observed in Nothofagus glauca (Phil.)
Threatened species are often characterized by small pop- Krasser (Burgos et al. 2008), the seeds in the soil can re-
ulation of mature individuals and reduced seed production establish and maintain the species population (Baskin and
(Fischer and Matthies 1998; Luijten et al. 2000). Plants Baskin 1978; Milberg 1994; Thompson et al. 1997).
with zoochoric mode of dispersal are particularly affected However, a reduced seed bank on the forest floor due to
by disturbances resulting in decreased pollen availability predation may affect the survival and mortality thus
and reduced seed set (Jennersten 1988; Lamont et al. 1993; resulting in reduced germination as observed in Phoebe
Ågren 1996). Limited seed production in Magnolia stellata bournei (Hemsl.) Yen C. Yang, a threatened and endemic
(Siebold & Zucc.) Maxim. was attributed to elevated pollen species of China (Darong and Bosun 2001) as well as M.
scarcity and genetic deterioration thus warranting manual schiedeana where seeds exposed to vertebrates resulted in
cross-pollination to maintain the population (Hirayama 100% seed removal (Vásquez-Morales and Sánchez-
et al. 2005). Similarly, in Talbotiella gentii Hutch. & Velásquez 2011). Similarly, in N. glauca, the microlepi-
Greenway, the natural reproduction was affected due to dopteran larva of Perzelia sp. is a pre-dispersal seed
processes between pollen germination and fruit and seed predator that emerges from August to November and
set, including pollen quality, fertilization rates, flower and coincides with the flowering of the species (Morales 1993;
fruit abortion, and resource limitation (Dompreh et al. Rojas 1996). The seeds are also attacked by post-dispersal
2015). Microhabitats and disturbance also play an impor- seed predators such as small mammals (Donoso et al.
tant role in influencing seed production. For instance, in M. 2004). Swietenia macrophylla King. produces 40–50 win-
dealbata, a high number of individuals were recorded in ged seeds per fruit on average and is classified as abundant
secondary succession forest characterized by greater flower in terms of seed production. However, Lamb (1966) cited
and fruit production as compared to those in pasture lands seed predation by parrots and macaws, while they were still
(Gutiérrez and Vovides 1997). on the trees and predation by different rodents on the forest
Seed banks are important sources of genetic reserves for ground. The closed fruits on the ground were often attacked
trees with semi-recalcitrant seed characteristics. The soil by termites as well. In the seedling stage, the attack of
seed bank is formed after viable seeds become buried in the yellow caterpillars (Steniscadia poliophaea) that destroyed
soil and litter, or accumulate on the ground surface the leaflets was common. Although the seeds, fruits and
(Simpson et al. 1989). Soil seed banks of individual species seedlings present different predation forms, the
vary significantly in length from transient to persistent microlepidopter (Hypsipyla grandella Zeller) attacking the

Author's personal copy
Ecology of seed germination in threatened trees: a review 193

apical branches was considered the major pest of S. Under natural conditions, the periodicity of rainfall
macrophylla. Thus, seed bank in the soil is dependent on plays an important role in determining the germination
seed set frequency, disturbance, predation, persistence as pattern of tree species. It also acts as a limiting factor for
well as seed type that ultimately determine the regeneration seed production and seedling survival (Fischer and
ability of the species. Matthies 1998; Luijten et al. 2000). In A. malaccensis, seed
production was limited to the monsoon (June to August)
2.3 Germination pattern season (Tabin and Shrivastava 2014) while germination
was initiated in Ilex khasiana Purk. with the onset of few
Following seed fall, the pattern of seed germination showers of rain in spring (March–April) season (Upadhaya
determines the recruitment of species. Although germina- et al. 2009). Seed moisture content is a major limiting
tion studies have been conducted under laboratory or factor in recalcitrant seeds as germination percentage is
controlled conditions, there is limited information from directly proportional to the seeds’ storage period. Bonner
field or natural conditions. Under natural environment, (1990) classified seeds into: ‘true orthodox’ seeds that can
seeds are dispersed across a wide variety of microhabitats be stored for long periods at moisture contents of 5–10%
covering a range of abiotic and biotic conditions which and sub-freezing temperatures; ‘sub-orthodox’ seeds that
affects their germination (Castro et al. 2005). Once seeds can be stored under the same conditions, but for shorter
are dispersed, the various physical and biotic characteris- periods; ‘temperate recalcitrant’ seeds that cannot be dried
tics, prevalent in the area act as a selective force in at all, but can be stored for 3–5 years at near-freezing
determining which species will germinate and establish temperatures and ‘tropical recalcitrant’ seeds that also
(Bazzaz 1991). Germination under field conditions can be cannot be dried, and they are killed by temperatures below
spatially and temporally variable, as some microhabitats 10–15 °C. However, some species exhibit semi-recalcitrant
may provide more favourable conditions than others characteristics when stored in appropriate conditions and
(Bisigato and Bertiller1999; Nilsson et al. 2000; Oleskog can remain viable for long periods, and they have been
and Sahlén 2000; Isselstein et al. 2002). Among environ- classified as semi-recalcitrant type. Such seeds require a
mental factors, a suitable combination of temperature, moist substratum and specific storage temperatures. In
moisture and light conditions are considered as key deter- terms of storage behaviour, of the total 78 species con-
minants of seed germination (Bewley and Black 1994; sidered in the present study, the seed type of 27 (35%)
Baskin and Baskin 1998). Raich and Khoon (1990) species were not available while 23 (30%) species had
investigated seed germination in a Dipterocarp forest under recalcitrant, 18 (24%) orthodox and 9 (12%) had semi-
three contrasting light conditions viz. forest understorey, recalcitrant seeds (‘‘Appendix’’ section).
gap and clearing and reported that the critically endangered Under controlled conditions, fairly high germination
D. grandiflorus and the endangered Vatica nitens King. percentages have been observed in some threatened trees
showed a germination percentage of 95% and 91% in forest having recalcitrant and intermediate seeds. For instance, B.
understorey and 33% and 5% in forest clearing, respec- ovalifoliolata germinated to a maximum of 70% (Savi-
tively. A similar trend in germination was observed in thramma et al. 2012), A. malaccensis—92% (Tabin and
Aquilaria malaccensis Lam., Canarium littorale Blume. Shrivastava 2014), G. canarica—90% (Keshavachandra
and Shorea multiflora (Burck) Symington, with high ger- and Krishnakumar 2016), Humboldtia laurifolia M.Vahl.—
mination in forest understorey. For, H. pandurifolia and 80% (Jayasuriya et al. 2010), H. pandurifolia—90% (Yu
Litsea pierrei H. Liu, two endangered trees, germination et al. 2008), Hyophorbe lagenicaulis (L.H.Bailey)
percentages of 28% and 54% in forest understorey and H.E.Moore—75% (Wood and Pritchard 2003), Myristica
17% and 21% in canopy gaps, respectively, were observed malabarica Lam—100% (Kumar et al. 2002), S. globulif-
in southwest China (Yu et al. 2008). Similarly, the criti- era—100%, (Corbineau and Côme 1989), S. asoca—80%
cally endangered Shorea trapezifolia (Thwaites) P.S. (Singh et al. 2005), Polylepsis besseri Hieron.—90%
Ashton, a rainforest dipterocarp endemic to Sri Lanka, had (Gareca et al. 2012). Seeds of A. malaccensis failed to
the highest germination of 83% in partial shade (de Zoysa germinate when stored for 15 days (Tabin and Shrivastava
and Ashton 1991). There is a certain affinity of tree seeds 2014). Seeds of G. canarica showed a maximum germi-
to germinate under shaded conditions. However, the seeds nation of 90% with an initial moisture content of 38% that
of I. griffithii (Mukhia 2006) and Alstonia macrophylla gradually declined after 70 days of storage (3% germina-
Wall.ex G.Don (Raich and Khoon 1990) exhibited germi- tion) when the moisture content reached 14% and failed to
nation percentages of 87% and 72% in forest gaps and germinate below this moisture level (Keshavachandra and
clearing and a low percentage of 3% and 27% in forest Krishnakumar 2016). Similarly, in Lophopetalum wight-
understorey, respectively. ianum Arn., the moisture content reduced to 9.21% after
30 days, and there was no germination, whereas at a

Author's personal copy
194 V. Iralu et al.

moisture content of 16%, germination of 84% was germination failure in many species (Bewley 1997). Baskin
observed in L. wightianum (Keshavachandra et al. 2014). A and Baskin (1998, 2004) defined ‘dormancy’ as the phe-
germination of 67% was observed in M. officinalis when nomenon by which seeds fail to germinate under conditions
the soil water content was 25% (Shu et al. 2010; Zhou et al. otherwise considered as favourable for germination. While
2012). Species vary significantly in their critical moisture many studies view seed dormancy as an obstacle in prop-
content that ranges between 12 and 31% (Ellis 1991; agation, it is, in fact, the adaptive mechanism that ensures
Tompsett 1991). In Hopea odorata Roxb dehydration the survival of the species through periods of environ-
below 24% inhibited germination (Corbineau and Côme mental stress under natural conditions (Gutterman 1993;
1989; Krishnapillay et al. 1991) and in H. pandurifolia, Baskin and Baskin 1998; Garcı́a-Gusano et al. 2004; Ker-
50% of the seeds lost their ability to germinate when mode 2005). Variation in dormancy between years has also
moisture content reduced to 12% (Yu et al. 2008). Kumar been suggested as an adaptation to unpredictable environ-
et al. (2002) reported 100% seed germination in M. mal- ments (Andersson and Milberg 1998). According to Phi-
abarica at moisture content of 27%. In M. dactyloides, the lippi (1993), seed germination rate can be affected by
critical moisture content was 34% (Sivakumar et al. 2006). humidity levels during seed maturation with drier envi-
The seeds of Poeciloneuron pauciflorum Bedd. are a rare ronments inducing higher dormancy (Qaderi and Cavers
and endemic tree species of the Southern Western Ghats of 2000). The intensity of seed dormancy and degrees of intra-
India, which when stored at room temperature (28–31 °C) specific variation depends upon several factors (Andersson
exhibited critical moisture content of 22% for germination, and Milberg 1998). Nikolaeva (1969, 1977) broadly clas-
above which 70–75% seed germination was recorded while sified seed dormancy under two general categories, i.e.
germination decreased to 46–58% when the moisture exogenous dormancy (i.e. outside the embryo) caused by
content dropped below 22% (Koilpillai 2017). The seeds of some physiological factors, characteristics of structures
Magnoliaceae such as Magnolia champaca (L.) Baill. ex including endosperm, seed coats, fruit walls, etc. (Niko-
Pierre are known to be recalcitrant or short-lived orthodox laeva 1977; Yang et al. 2007) and endogenous dormancy
and require high moisture to maintain viability (Bahuguna attributed to some characteristics of the embryo, the pres-
et al. 1987; Robbins 1988; Bisht and Ahlawat 1999). In ence of the hard seed testa (morphological seed dormancy)
Swietenia mahagoni seeds stored at 2–5 °C with 4–5% or germination inhibitors present in the capsules or endo-
moisture content are viable up to 1 year (Schmidt and sperm (Nikolaeva 1977; Hilhorst et al. 2006). Seed ger-
Jøker 2000). In natural conditions, the depth of burial also mination failure is attributed to the presence of either
plays an important role in preserving seeds with semi- factor. However, in some seeds, both endogenous and
orthodox characteristics as reported for M. schiedeana exogenous seed dormancy may be present (Bewley and
(Vásquez-Morales and Sánchez-Velásquez 2011) and M. Black 1994).
dealbata (Corral-Aguirre and Sanchez-Velasquez 2006). Physical and mechanical dormancy are the most com-
Thus, both environmental factors (light, moisture) as well mon inhibitors of germination in many seeds. Families like
as seed storage behaviour are known to determine the Leguminosae, Cannaceae, Malvaceae, Convolvulaceae and
pattern of seed germination in tree species. Although par- Fabaceae exhibit exogenous dormancy due to an imper-
tial light and shaded conditions have been reported to be meable seed coat (Whelan 1995). Some tree species such
favourable for some species, others have an affinity toward as Cupressus atlantica Gaussen (Youssef et al. 2012),
forest gaps and clearings. In terms of storage behaviour, Elaeocarpus blascoi Weibel (Ramasubbu and Irudhyaraj
recalcitrant seeds fail to germinate below a critical soil and 2016), Intsia bijuga (Colebr.) Kuntze (Thaman et al. 2006)
seed moisture content, whereas some species exhibiting exhibit exogenous dormancy. In such species, water pen-
semi-recalcitrant characteristics when stored in appropriate etration required for embryo growth and expansion is
conditions can remain viable for long periods. Seeds of inhibited by the hard seed coats. Mechanical dormancy
Lysiloma acapulcense (Kunth) Benth., collected from four induced by seed coat impermeability is known to cause low
sites in the tropical dry forest of Morelos, Mexico, showed and erratic germination and is usually associated with the
significant differences in seed size and germination among presence of one or more layers of impermeable palisade
provenances in the species. Germination capacity of stored layers of lignified cells (Vazquez Yanes and Perez Garcia
seeds (24 months) was still C 50% in all provenances 1976; Corner 1976). The presence of galactomannan
(Cervantes and Bonfil 2014). polymers on the walls of the endosperm in the seeds of
Gymnocladus assamicus P.C.Kanjilal (Choudhury et al.
2.4 Seed dormancy 2009) has been attributed to its highly impermeable nature
(McCleary and Matheson 1974). Species with hard seed
Apart from the physical factors (moisture, light, substratum coats can remain dormant for a period of few months as
etc.), seed dormancy contributes significantly to

Author's personal copy
Ecology of seed germination in threatened trees: a review 195

observed in P. africana (Negash 2004) to as long as 5 years existence of a physiological dormancy (Baskin and Baskin
as reported in C. atlantica (Youssef et al. 2012). 1998).
Endogenous dormancy is found in a number of plant A new type of dormancy in Humboldtia laurifolia M.
families such as Apiaceae, Aquifoliaceae, Araceae, Ara- Vahl characterized by considerably delayed plumule (ca.
haceae, Aristolochiaceae, Berberidaceae, Fumariaceae, 50 days) and radicle emergence (within 18 days) was
Illiciaceae, Lardizabalanceae, Liliaceae, Magnoliaceae, observed (Jayasuriya et al. 2010). The epicotyl elongated
Papaveraceae, Ranunculaceae and Schisandraceae very slowly with a length of * 15–17% of that of the seed
(Grushvitzky 1967). There are insufficient studies in fam- at the beginning of plumule growth which increased to
ilies with underdeveloped embryo, thus limiting the 23–25% at the time of shoot emergence. The dormancy in
knowledge of whether seeds have morphological or mor- this species was attributed to the epicotyl and later classi-
pho-physiological dormancy (Baskin and Baskin 1998). fied as non-deep physiological dormancy of the plumule.
Morphological dormancy has been documented in only two Though failure in seed germination is attributed to the
temperate families, i.e. Apiaceae and Ranunculaceae presence of either exogenous or endogenous seed dor-
(Baskin and Baskin 1998). In the present review, most of mancy or both and is viewed as an obstacle in propagation,
the species exhibited morpho-physiological dormancy it is in fact an adaptive strategy that ensures the survival of
(MPD). Magnoliaceae members viz. M. punduana (Iralu the species through periods of environmental stress under
and Upadhaya 2016), M. schiedeana (Vásquez-Morales natural conditions.
and Sánchez-Velásquez 2011), M. ingrata (B.L.Chen &
S.C.Yang) Figlar (Han and Long 2010), Michelia yunna- 2.5 Overcoming seed dormancy
nensis (Hu) Noot. (Han et al. 2010), Manglietiastrum
sinicum Y.W. Law (Zheng and Sun 2009) and Magnolia Depending on the type of dormancy present in seeds,
grandis (Hu & W.C.Cheng) V.S. Kumar (Pan and Sun various treatments have been applied for overcoming dor-
2009), have underdeveloped embryos at the time of mat- mancy. Some of the most common techniques used are
uration indicating the presence of morpho-physiological listed below:
dormancy. In M. punduana, the embryos were small and
1. Scarification, which can be of two types viz. mechan-
differentiated into cotyledons and radicle that continued to
ical and chemical. In the former, the hard seed coat is
grow inside the seeds after dispersal (Iralu and Upadhaya
cracked open or subjected to physical abrasion whereas
2016). The seeds of M. dealbata have been thought to
in the latter, seeds are soaked in concentrated acid for
exhibit exogenous dormancy caused by oils and inhibitors
specific amount of time depending on the thickness of
of the sarcotesta and lignified testa (Vovides and Iglesias
the testa.
1996). However, endogenous dormancy and natural ger-
2. Stratification (seeds subjected to chilling)
mination after 9 months of seed dispersal were reported by
3. Storage conditions (temperature, moisture and
Corral-Aguirre and Sanchez-Velasquez (2006) in Mexico.
This revealed that seeds of M. dealbata are subjected to a
4. The application of gibberellins (GA3) can overrule
natural cold stratification when exposed to 10–20 days of
photodormancy, thermodormancy, dormancy imposed
frost per year (Zulueta–Rodrı́guez and Soto 1993). Similar
by incomplete embryo development, mechanical bar-
results on natural stratification have been reported in M.
riers and the presence of germination inhibitors
punduana (Iralu and Upadhaya 2016) whereby low tem-
(Bewley and Black 1994).
peratures gradually release the nutrient reserves of the
endosperm for the growth of the embryo, allowing its A combination of treatments can also be used in
survival during winter (Camacho 1994). breaking dormancy. A brief review of each of the dor-
The germination of seeds in Pritchardia remota mancy-breaking techniques applied in most of the species
(Kuntze) Becc. (Perez et al. 2008) and Podocarpus has been summarized as follows:
angustifolius Griseb. was delayed by 4 weeks due to MPD
induced by the presence of a lineal and rudimentary 2.5.1 Scarification
underdeveloped embryo (Ferrandis et al. 2011), while, in I.
paraguariensis, MPD was attributed to the woody endo- Many species exhibit physical impediments to water per-
carp as whole pyrenes failed to germinate even after meability imposed by the presence of hard seed coat.
120 days as opposed to bisected pyrenes that germinated Species belonging to Leguminosae, Cannaceae, Mal-
successfully (Almeida et al. 2000; Dolce et al. 2010). The vaceae, Convolvulaceae and Elaeocarpaceae are charac-
seeds of P. angustifolius needed an additional 9 days to terized by an impermeable seed coat. The hard seed coat
achieve a high value of germination suggesting the may confer tolerance to heat (Whelan 1995). Under natural
conditions, fire plays a key role in regeneration where it

Author's personal copy
196 V. Iralu et al.

cracks the seed coats and promotes germination (Baskin germination. Dormancy can also be broken by water sub-
and Baskin 1998) and induces the release of other chemical mersion and temperatures fluctuations in certain species as
components that are known to stimulate seed germination well as scarifying. However, various combinations of
(Van Staden et al. 2000; Hilhorst et al. 2006). Seeds of mechanical scarification and hot water treatment (Baikiaea
Quercus robur L. when exposed for 10 and 15 min to plurijuga and G. assamicus); hydropriming and biopriming
smoke and charcoal had a germination percentage of (A. hickelii and A. religiosa) cold stratification (M. schie-
90–94% (Reyes and Casal 2006). Seeds of S. macrophylla deana) and soaking in water of varying temperature (C.
had a cumulative germination of 13% after slash, fell and atlantica) can significantly improve germination.
burn treatment (Negreros-Castillo et al. 2003). Subjecting
seeds to varying periods of water submersion and tem- 2.5.2 Stratification
peratures fluctuations can break dormancy in certain spe-
cies. Scarification of seeds by nicking a part of the seed Stratification of seeds to varying periods of chilling is
coat or by rubbing the seeds against a rough surface is known to break dormancy especially in species exhibiting
known to increase germination in many species. Germi- MPD. Seeds of M. dealbata stratified in barren humid sand
nation percentage ([ 67%) in seeds of C. atlantica was exposed to a chilling temperature of 4–10 °C and sub-
obtained upon hand scarification with sand paper (Youssef merged for 24 h in room temperature (18–20 °C) yielded a
et al. 2012). When soaked in water at a temperature of germination of 100% (Corral-Aguirre and Sanchez-Ve-
60 °C and 80 °C for 15 min, seeds of this species germi- lasquez 2006). Cold stratified seeds of M. yunnanensis
nated to 34% and 67%, respectively, in comparison to the germinated to 89% and 71% after 80 and 100 days of
control (18%). Nicked seeds of T. mucronatum placed on stratification, respectively (Han et al. 2010). Similarly, cold
moist filter paper showed germination of about 14% (Hi- stratification for 90 days yielded high germination (93%)
laire 2001). The seeds of Baikiaea plurijuga Harms showed in Magnolia punduana (Iralu and Upadhaya 2016),
75% germination upon mechanical scarification, and 100% whereas M. grandis attained highest germination after
germination upon hot water pre-soaking for 9 min, whereas 60 days (Pan and Sun 2009). Seeds of Picea omorika
chemical scarification of the seeds in 98% H2SO4 for more (Pancic) Purk. required a temperature of 4 °C for ca.
than 3 min drastically reduced germination percentage. 6 weeks for germination (Gosling 2007). However, in
The seeds of this species have a weak seed coat and some species cold stratification resulted in no germination.
required pre-soaking in hot water (Botsheleng et al. 2014). Seeds of M. dactyloides stored at a low temperature
Similarly, in G. assamicus mechanical scarification and hot (0–5 °C) failed to germinate probably due to cell damage
water treatment improved germination significantly by or the formation of ice crystal within cells (Bewley and
65–80%, while untreated seeds showed 42% germination. Black 1994). Although cold stratification to varying peri-
Chemical scarification of the seeds in concentrated H2SO4 ods of chilling is known to overcome dormancy, it may
for 40 min also increased the germination to [ 55% also result in germination failure.
(Choudhury et al. 2009).
A combination of hydropriming (sterile distilled water 2.5.3 Light, temperature, and substratum
with a constant supply of oxygen) and biopriming using
rhizobacteria Pseudomonas fluorescens and Bacillus sub- Extrinsic factors such as light, temperature and a growing
tilis strain on the germination of two endangered fir Abies substratum may substantially affect seed germination and
hickelii Flous & Gaussen and A. religiosa resulted in 91% seedling survival (Bargali et al. 1998; Everham et al.
and 68% germination, respectively (Zulueta-Rodrı́guez 1996). High germination in seeds of Jacaranda mimosifo-
et al. 2015). Similarly, in M. schiedeana, a combination of lia D.Don was observed in both light and dark conditions at
mechanical scarification, cold stratification at 4–10 °C and a temperature of 25 °C (Socolowski and Takaki 2004).
soaking in water of varying temperature improved seed Seeds of Picconia azorica (Tutin) Knobl., when stored at
germination to 84% (Vásquez-Morales and Sánchez- low temperature (10/5 °C) followed by warm stratification,
Velásquez 2011). On the other hand, manual scarification germinated successfully, thus suggesting that warm tem-
reduced germination in M. punduana to 20% (Iralu and perature contributes to embryo development (Martins et al.
Upadhaya 2016) whereas manual aril removal increased 2012). Seeds of M. dactyloides when stored in different
the germination of Magnolia pugana (H.H. Iltis & Vaz- substratum for 3 months at 20 °C showed high germination
quez) A. Vazquez & Carvajal to 52% (Jacobo-Pereira et al. in germination paper (88%) in comparison to moist ver-
2016). Thus, physical dormancy imposed by the presence miculite, mineral soil, sand, sponge sheet and cotton towel
of structural impediments can be overcome by various (Sivakumar et al. 2006). A pre-treatment of soaking seeds
exogenous factors such as fire that induces the release of in hot water for 15 min and thereafter sowing in a sub-
other chemical components known to stimulate seed 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 197

sawdust resulted in 92% germination in Milicia excelsa In addition to soil temperature and moisture, seed ger-
(Wele.) C.C. Berg. (Nzekwe et al. 2013). Bannister et al. mination is also affected by light intensity. Germination of
(2014) reported that moist substrates composed of sphag- P. sylvetris under field conditions was highest (95%) in
num or mineral soil were best suited for seed germination shade-free microhabitats and high soil temperature (mean
of P. uviferum (ca. 60%). A combination of chemical max—21 °C), while germination was delayed under low
scarification in H2SO4 followed by culture on solid nutrient light intensity (Nyman 1963; Tillberg 1992). The optimum
medium resulted in a germination of 86–94% in Maytenus temperature for Nyssa yunnanensis W.Q. Yin ex H.N. Qin
canariensis (Loes.) G. Kunkel & Sunding (Gutiérrez-Ni- & Phengklai was 25 °C. The seeds germinated better in
colás et al. 2008). Padmalatha and Prasad (2007) reported light (12 h/day) than in dark treatment (Yuan et al. 2013).
that under in vitro conditions, seeds of the endangered tree The effect of different light intensity and soil moisture on
Pterocarpus santilinus L.f. when soaked overnight in tap the seed germination of Parashorea chinensis Wang Hsie
water followed by mechanical scarification resulted in revealed that 40% light and 60% soil moisture was opti-
100% germination on Murashige and Skoog-MS (liquid) mum for germination (Xiaojin 2015). However, seed ger-
medium. Seeds of P. alba exhibited low germination per- mination and seedling establishment of M. patungensis,
centages at low temperature (10/5 °C), whereas at high- under four soil types and three shade treatments (0%, 40%
temperature regimes (20/10 °C, 25/15 °C and 35/20 °C), and 80% of full sunlight) showed that germination rate was
seeds from all the provenances showed high germination low (19–31%) and soil type had no significant effect on
percentages (Venier et al. 2015). Similar observations were seed germination rate. Seedling survival and growth rate
made in Prosopis caldenia Burkart where a high temper- increased with increasing light intensity and also promoted
ature applied for few minutes promoted seed germination biomass accumulation and root development. The seedling
(de Villalobos et al. 2002). Alternating temperature of 20° survival rate was highest (91%) in the farmland soil but
and 30 °C resulted in 65% germination in M. officinalis, reduced to 80%, 78% and 53% in old-field soil, sandy soil
whereas a temperature of 20° and 10 °C was favourable for and forest soil, respectively (Chen et al. 2012). In the
M. grandis with 36% germination. A temperature of present study, seeds of nine species were positively pho-
22.3 °C was optimum for the germination of P. besseri and toblastic and responded to light treatment. Thus, varying
fluctuating the temperature between 20/10 °C resulted in periodicities and intensities of light condition, temperature
93% germination (Gareca et al. 2012). Asomaning et al. as well as a growing substratum affect seed germination in
(2010) reported that the germination of Khaya anthotheca many tree species.
(Welw.) C. DC. showed better response at 20 °C and 30 °C
and alternating the temperature regimes at 5/30 °C, 2.5.4 Plant growth regulators
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 Plant hormones are known to regulate many physiological
performed best under alternating temperatures of 10/5 °C and bio-chemical processes in plant. Some of the mecha-
and 15/10 °C with a germination of 62% (Martins et al. nisms controlled by growth regulators include cell division,
2012). Seeds of S. globulifera and Pterogyne nitens Tul. growth and differentiation (Hooley 1994) and seed dor-
showed better germination at higher temperatures mancy and germination (Graeber et al. 2012). Abscisic acid
(20–35 °C) (Corbineau and Côme 1989; Morandini et al. (ABA) inhibits cell cycle (Sanchez et al. 2005) and initiates
2013). Studies on the germination of Eriotheca vargasii dormancy (Groot and Karssen 1992) and hence, ABA
(Cuatrec.) A. Robyns (Malvaceae), an endemic Peruvian deficient seeds exhibit rapid germination. Nitrates in plants
Andean tree, revealed that substrate moisture levels had no can act as a source of nitrogen as well as enhance seed
influence on germination capacity or rate. However, tem- germination (Atia et al. 2009). Plant hormones like ethy-
perature (25 °C) and substrate type (commercially pre- lene and gibberellins affect radicle growth. Gibberellins are
pared media) showed strong effects on germination (90%) the most important for the production of mannanase which
(Mamani et al. 2018). Thus, one of the most effective is necessary for seed germination (Wang et al. 2005) as it
treatments for germination was incubation of seeds in stimulates the synthesis and production of the hydrolases,
different temperature regimes as observed in 19 species. especially a-amylase, resulting in seed germination (Ap-
Some species either responded to a constant temperature pleford and Lenton 1997; Yamaguchi 2008) by inhibiting
treatment (P. besseri) or a fluctuating temperature regime ABA activity. Auxins (IAA) also play a key role in regu-
(P. alba, S. globulifera, Pterogyne nitens Tul., and M. lating cell cycling, growth and development, formation of
grandis), whereas others (P. remota, M.schiedeana) vascular tissues (Davies 2013) and pollen (Ni et al. 2002)
exhibited successful seed germination on incubation in and development of other plant parts (He et al. 2000).
combination with mechanical treatment. External application of GA3 in M. sinicum showed a ger-
mination of 66% when the seeds were soaked for 24 h in

Author's personal copy
198 V. Iralu et al.

500 mg L-1 GA3. Application of GA3 along with light was The use of PGRs (GA3, IAA, IBA SNPs etc.) and cold
useful in breaking dormancy in S. album (Das and Tah stratification in combination with an incubation treatment
2013; Vijayan and Rahees 2015). Seeds of M. yunnanensis was found to be effective for breaking dormancy and
soaked in 2000 mg L-1 GA3 for 48 h germinated to 94% at enhancing germination in many species (M. sinicum, M.
a temperature of 25 °C and 20/25 °C (Han et al. 2010). yunnanensis and M. punduana). However, the selection of
Similarly, GA3 induced germination has been reported in the combination of various growth hormones, substratum
M. punduana where seeds soaked in 3000 mg L-1 GA3 and and growth conditions needs to be evaluated that may vary
incubated at 25 °C germinated to 77% (Iralu and Upadhaya with seed type.
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 3 Conclusion
Upadhaya 2018). GA3 induced faster germination in C.
atlantica at 1000 and 2000 mg L-1 (Youssef et al. 2012). The present investigation revealed that the major threats to
Sivakumar et al. (2006) reported that application of the decline of threatened species is attributed but not
1000 ppm GA3 (ca. 63.5%) as well as 1000 ppm IBA confined to extraction of timber and Non-Forest Timber
(94.5%) initiated germination of M. dactyloides seeds Products (NTFPs) with a concomitant poor natural regen-
stored at 15 or 20 °C for 3 months. The comparatively eration. Other factors such as habitat degradation, poor
significant effect of indoleacetic acid (IAA) than naph- regeneration and low population also contributed in part to
thylacetic acid (NAA) on the seed germination of Jacar- the decline of the species. The formation of seed banks in
anda mimosifolia D. Don when kept in an illumination the soil can be viewed as a strategy for species persistence
incubator at 25 °C/18 °C under 15 h light was reported by in nature especially for those with low natural population.
Zhou et al. (2012). The seeds of endangered tree Mansonia Majority of the species exhibited orthodox seeds and
altissima (A.Chev) A.Chev. when soaked in 0.02 g L-1 required a pre-treatment for germination. Temperature
IAA for 24 h and sown in a substratum of washed river played a major role as an effective treatment for initiating
sand showed a germination of 66% and 0.01 g L-1 and germination in many of the species. Furthermore, the use of
0.03 g L-1 IAA had a germination of 62%. Indole-3-bu- PGRs (GA3, IAA, IBA SNPs, etc.) and cold stratification in
tyric acid (IBA) treatment of 0.02 g L-1 also yielded 62% combination with an incubation treatment was found to be
germination but low concentration reduced germination to effective for breaking dormancy and improving germina-
38% (Maku et al. 2014). The application of nitrate (KNO3) tion. However, the present review revealed that there is
did not promote germination of M. yunnanensis (Han et al. limited literature on the germination requirements of many
2010) and E. prunifolius (Iralu and Upadhaya 2018) seeds. of the threatened species indicating lacunae in the field of
Similarly, seeds treated solely with KNO3 resulted in low germination ecology. The findings highlight and emphasize
germination (16%) in M. punduana (Iralu and Upadhaya the need for detailed knowledge of seed structures and
2016) and 2% in P. santilinus (Padmalatha and Prasad factors affecting the growth potential of the embryo to
2007). A combination treatment of GA3 and alternating enable development of dormancy-breaking techniques. In
temperature (10–40 °C) improved germination of Ptero- addition, methods of seed handling, storage behaviour and
carpus angolensis DC (van Daalen 1991). In B. ovalifoli- germination of many threatened species are emphasized to
olata, application of silver nanoparticles (SNPs) had a prevent extinction risks. Development of guidelines for
significant effect on germination. Seeds planted in MS ecosystem management via seed germination protocols
medium with different concentration of SNPs exhib- will help maintain biodiversity values in ecological sys-
ited [ 90% germination with the highest in 30 lg ml-1 tems and aid the conservation of threatened species.
(Savithramma et al. 2012). The high germination has been
Compliance with ethical standards
attributed to the penetrating property of SNPs into the seed
coats resulting in embryo activation. The dormancy in Si- Conflict of interest All authors declare that they have no conflict of
nojackia xylocarpa Hu was broken by a combination interest.
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 Appendix
removal of fleshy endocarp and subsequent treatment in
GA3, leached drupes treated with GA3, seeds scarified in See Table 1.
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.

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)
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
monoculture of
exotic tree
Elaeocarpus Subtropical Habitat VU Cosexual Drupe Zoochory O ND Ca 2 years Iralu and Upadhaya
prunifolius degradation (2018)
Eriotheca vargasii Seasonally dry EN Cosexual Capsule Anemochory ND ND ND Mamani et al. (2018)

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)

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
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
Hyophorbe Tropical Regeneration is CR Monoecious Nut NA R Dried seeds, higher ND Wood and Pritchard
lagenicaulis sporadic, light intensity (2003)
Arecaceae restricted
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)
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
Lophopetalum Tropical Exploited for LR/ Dioecious Capsule Anemochory R Sand bed 20–30 days Keshavachandra et al.
wightianum perupok timber LC (2014)
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

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)
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)

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
Magnolia Subtropical and ND DD Cosexual Follicle Zoochory SR Plant growth hormones ND Han et al. (2010)
yunnanensis Temperate (GA3), Cold
Magnoliaceae stratification,

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)

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
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
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,
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/
Nothofagus glauca Temperate Habitat converted VU Monoecious Nut Zoochory R ND ND Burgos et al. (2008)
Nothofagaceae into Pinus
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
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,
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
Podocarpus Tropical Fire, mining VU Dioecious Drupe Autochory/ SR ND ND Ferrandis et al. (2011)
angustifolius Zoochory
Poeciloneuron Tropical and Timber extraction, CR Dioecious Capsule NA R No treatments required ND Koilpillai (2017)
pauciflorum Subtropical habitat loss
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
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

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)

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
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
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
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
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)
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
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
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
Swietenia Tropical and Most important VU Monoecious Capsule Anemochory R 80% light ND Negreros-Castillo
macrophylla Temperate commercial et al. (2003)
Meliaceae mahagony, poor
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-
Talbotiella gentii Tropical dry Low population, CR Cosexual Pods Ballochory ND ND ND Dompreh et al. (2015)
Fabaceae charcoal and fuel
Author's personal copy

Taxodium Riparian Timber value LC Monoecious Cone Anemochory ND Mechanical ND Hilaire (2001)
mucronatum scarification
Ternstroemia Tropical Habitat loss VU Dioecious Berry Zoochory ND Studied under natural ND Raich and Khoon
wallichiana conditions (1990)
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

Author's personal copy
206 V. Iralu et al.

References Bisht NS, Ahlawat SP (1999) Seed technology. SFRI Information

Bulletin No. 7. State Forest Research Institute, Itanagar
Ågren J (1996) Population size, pollinator limitation, and seed set in Bisigato AJ, Bertiller MB (1999) Seedling emergence and survival in
the self-incompatible herb Lythrum salicaria. Ecology contrasting soil microsites in Patagonian Monte shrubland. J Veg
Sci 10:335–342
Ahmed AIMU (2008) Underlying causes of deforestation and forest Bonner FT (1990) Storage of seeds: potential and limitations for
degradation in bangladesh. A Report Submitted to the Global germplasm conservation. For Ecol Manag 35:35–43
Forest Coalition (GFC), The Netherlands Botsheleng B, Mathowa T, Mojeremane W (2014) Effects of pre-
treatments methods on the germination of pod mahogany
Alexander H, Cummings C, Kahn L, Snow A (2001) Seed size
variation and predation of seeds produced by wild and crop–wild (Afzelia quanzensis) and mukusi (Baikiaea plurijuga) seeds. Int
sunflowers. Am J Bot 88:623–627 J Innov Res Sci Eng Technol 3(1):8108–8113
Almeida JP, Zanatta B, Winge H (2000) Effect of the endocarp on the Burgos A, Grez AA, Bustamante RO (2008) Seed production, pre-
germination of maté tree (Ilex paraguariensis A. St. Hil., dispersal seed predation and germination of Nothofagus glauca
Aquifoliaceae) seeds. In: Winge H (ed) Annals II Congresso (Nothofagaceae) in a temperate fragmented forest in Chile. For
Sul–Americano da Erva–Matee III Reunião Técnica da Erva– Ecol Manag 255:1226–1233
Mate, pp 427–431 Camacho M (1994) Dormicion de semillas. Causas y tratamientos
Andersson L, Milberg P (1998) Variation in seed dormancy among (No. 631.531 C1401d Ej. 1 005438). Trillas
mother plants, populations and years of seed collection. Seed Sci Cascante A, Quesada M, Lobo JJ, Fuchs EA (2002) Effects of dry
Res 8:29–38 tropical forest fragmentation on the reproductive success and
genetic structure of the tree Samanea saman. Conser Biol
Appleford NEJ, Lenton JR (1997) Hormonal regulation of a-amylase
gene expression in germinating wheat (Triticum aestivum) 16(1):137–147
grains. Physiol Plant 100:534–542 Castro J, Zamora R, Hódar JA, Gómez JM (2005) Ecology of seed
Asomaning JM, Sacande M, Olympio NS (2010) Germination germination of Pinus sylvestris L. at its southern, Mediterranean
responses of Khaya anthotheca seeds to a range of alternating distribution range. For Syst 14(2):143–152
and constant temperatures provided by the 2-way grant’s Cervantes M, Bonfil C (2014) Germination of stored seeds of four tree
thermogradient plate. Ghana J For 26:74–88 species from the tropical dry forest of Morelos, Mexico. Bot Sci
Atia A, Debez A, Barhoumi Z, Smaoui A, Abdelly C (2009) ABA 92(2):281–287
GA3, and nitrate may control seed germination of Crithmum Chacoff NP, Aizen MA (2006) Edge effects on flower-visiting insects
maritimum (Apiaceae) under saline conditions. C R Biol in grapefruit plantations bordering premontane subtropical
332:704–710. https://doi.org/10.1016/j.crvi.2009.03.009 forest. J Appl Ecol 43(1):18–27
Chen F, Liu L, Chen F, Jia G (2012) The ecological characteristics of
Atkinson IAE, Cameron EK (1993) Human influence on the terrestrial
biota and biotic communities of New Zealand. Trends Ecol Evol seed germination and seedling establishment of Manglietia
8(12):447–451 patungensis: implication for species conservation. Am J Plant
Baguette M, Schtickzelle N (2003) Local population dynamics are Sci 3(10):1455–1461
Choudhury BI, Khan ML, Das AK (2009) Seed dormancy and
important to the conservation of metapopulations in highly
fragmented landscapes. J Appl Ecol 40(2):404–412 germination in Gymnocladus assamicus: an endemic legume tree
Bahuguna VK, Rawat MMS, Naithani KC (1987) Investigation on the from Northeast India. Seed Sci Technol 37:582–588
seed of Michelia champaca Linn. for perfection of optimum Coder KD (2008) Tree sex: gender and reproductive strategies. Tree
conditions of storage. Indian Forester 113:243–248 selection series. Warnell School, University of Georgia, Athens
Baker HG (1989) Some aspects of the natural history of seed banks. Corbineau F, Côme D (1989) Germination and storage of recalcitrant
In: Leck MA, Parker VT, Simpson RL (eds) Ecology of soil seed seeds of some tropical forest tree species. Ann Sci For 46:89–91
banks. Academic, San Diego, pp 9–21 Corner EJH (1976) The seeds of dicotyledons, vol I–II. Cambridge
Bannister JR, Wagner S, Donoso PJ, Bauhus J (2014) The importance University Press, Cambridge
of seed trees in the dioecious conifer Pilgerodendron uviferum Corral-Aguirre J, Sanchez-Velasquez LR (2006) Seed ecology and
for passive restoration of fire disturbed southern bog forests. germination treatments in Magnolia dealbata: an endangered
species. Flora 201:227–232
Austral Ecol 39:204–213
Bargali K, Singh SP, Singh RP (1998) Seed characteristics and Darong W, Bosun W (2001) Seed and seedling ecology of the
germination behaviour of some early and late successional tree endangered Phoebe bournei (Lauraceae). Acta Ecol Sin
species on a nutrient gradient. Indian Forester 124:247–251 21(11):1751–1760
Baskin CC, Baskin JH (1998) Seeds. Ecology, biogeography and Das SC, Tah J (2013) Effect of GA3 on seed germination of Sandal
evolution of dormancy and germination. Academic Press, San (Santalum album L.). Int J Curr Sci 8:79–84
Diego Davies PJ (2013) Plant hormones: physiology, biochemistry and
Baskin JM, Baskin CC (1978) The seed bank in a population of an molecular biology. Springer, Berlin
endemic plant and its ecological significance. Biol Cons de Villalobos AE, Peláez DV, Bóo RM, Mayor MD, Elia OR (2002)
14:125–130 Effect of high temperatures on seed germination of Prosopis
Baskin JM, Baskin CC (2004) A classification system for seed caldenia Burk. J Arid Environ 52(3):371–378
de Zoysa ND, Ashton MS (1991) Germination and survival of Shorea
dormancy. Seed Sci Res 14:1–16
Bazzaz FA (1991) Habitat selection in plants. Am Nat 137:116–130 trapezifolia: effects of dewinging, seed maturity, and different
Berjak P, Pammenter NW (2004) Recalcitrant seeds. In: Benech- light and soil microenvironments. J Trop For Sci 4(1):52–63
Arnold RL, Sánchez RA (eds) Handbook of seed physiology, Didham RK (1997) The influence of edge effects and forest
fragmentation on leaf litter invertebrates in central Amazonia.
application to agriculture. Haworth Press, New York, p 480
Bewley DJ (1997) Seed germination and dormancy. Plants Cell In: Laurance WF, Bierregaard RO Jr (eds) Tropical forest
9:1055 remnants: ecology, management, and conservation of frag-
Bewley JD, Black M (1994) Seeds: physiology of development and mented communities. University of Chicago Press, Chicago,
germination. Plenum, New York, p 445 pp 55–70

Author's personal copy
Ecology of seed germination in threatened trees: a review 207

Dolce NR, Mroginski LA, Rey HY (2010) Endosperm and endocarp Hirano RT (1990) Propagation of Santalum, Sandalwood tree. In:
effects on the Ilex paraguariensis A. St.–Hil. (Aquifoliaceae) Hamilton L, Conrad CE (eds) Proceedings of the symposium on
seed germination. Seed Sci Technol 38:441–448 sandalwood in the Pacific, 9–11, April 1990, Honolulu, Forest
Dompreh D, Swaine MD, Wilcock CC (2015) Reproductive biology Service General Technical Paper PSW-122, pp 43–45
of the critically endangered tropical tree Talbotiella gentii. South Hirayama K, Ishida K, Tomaru N (2005) Effects of pollen shortage
For 77(2):153–163 and self-pollination on seed production of an endangered tree,
Donoso DS, Grez AA, Simonetti JA (2004) Effects of forest Magnolia stellata. Ann Bot 95:1009–1015
fragmentation on the granivory of differently sized seeds. Biolog Hooley R (1994) Gibberellins: perception, transduction and
Cons 115(1):63–70 responses. Plant Mol Biol 26:1529–1555
Ellis RH (1991) The longevity of seeds. HortScience 26:1119–1125 Iralu V, Upadhaya K (2016) Dormancy, storability and germination of
Everham EM, Myster RW, Vandegenachte E (1996) Effects of light, seeds in Magnolia punduana (Magnoliaceae). Botany
moisture, temperature, and litter on the regeneration of five tree 94:967–973. https://doi.org/10.1139/cjb-2016-0056
species in the tropical montane wet forest of Puerto Rico. Am J Iralu V, Upadhaya K (2018) Seed dormancy, germination and
Bot 83:1063–1068 seedling characteristics of Elaeocarpus prunifolius Wall. ex
Ferrandis P, Bonilla M, Osorio LC (2011) Germination and soil seed Müll. Berol.: a threatened tree species of Northeast India. N Z J
bank traits of Podocarpus angustifolius (Podocarpaceae): an For Sci 48:16. https://doi.org/10.1186/s40490-018-0121-y
endemic tree species from Cuban rain forests. Rev Biol Trop Isselstein J, Tallowing JRB, Smith REN (2002) Factors affecting seed
59(3):1061–1069 germination and seedling establishment of fen-meadow species.
Fischer M, Matthies D (1998) Experimental demography of the rare Restor Ecol 10:173–184
Gentianella germanica: seed bank formation and microsite IUCN (2016) The IUCN red list of threatened species. Version
effects on seedling establishment. Ecography 21:269–278 2016-2. www.iucnredlist.org
Garcı́a-Gusano M, Martinez-Gomez PM, Dicenta F (2004) Breaking Jacobo-Pereira C, Romo-Campos R, Flores J (2016) Seed germination
seed dormancy in almond (Prunus dulcis (Mill.) D.A. Webb). of Magnolia pugana (Magnoliaceae), an endemic and endan-
Sci Hortic 99:363–370 gered species from Western Mexico. Bot Sci 94(3):575–584
Gareca EE, Vandelook F, Fernández M, Hermy M, Honnay H (2012) Jayasuriya GKMG, Wijetunga ASTB, Baskin JM, Baskin CC (2010)
Seed germination, hydrothermal time models and the effects of Recalcitrancy and a new kind of epicotyl dormancy in seeds of
global warming on a threatened high Andean tree species. Seed the understory tropical rainforest tree Humboldtia laurifolia
Sci Res 22(4):287–298 (Fabaceae, Ceasalpinioideae). Am J Bot 97(1):15–26
Gosling P (2007) Raising trees and shrubs from seed. Forestry Jennersten O (1988) Pollination in Dianthus deltoids (Caryophyl-
Commission Practice Guide, Forestry Commission, Edinburgh laceae): effects of habitat fragmentation on visitation and seed
Graeber K, Nakabayashi K, Miatton E, Leubner-Metzger G, Soppe set. Cons Biol 2(4):359–366
WJ (2012) Molecular mechanisms of seed dormancy. Plant Cell Kermode AR (2005) Role of abscisic acid in seed dormancy. J Plant
Environ 35:1769–1786. https://doi.org/10.1111/j.1365-3040. Growth Regul 24:319–344
2012.02542.x Keshavachandra K, Krishnakumar G, Shenoy HS (2014) Seed
Grandtner MM (2005) Elsevier’s dictionary of trees. Volume 1: North germination studies on Lophopetalum wightianum Arn.—an
America. Elsevier, Amsterdam evergreen species of the Western Ghats. Int J Plant Anim
Groot SP, Karssen CM (1992) Dormancy and germination of abscisic Environ Sci 4(3):502–507
acid-deficient tomato seeds: studies with the sitiens mutant. Plant Keshavachandra K, Krishnakumar G (2016) Seed germination studies
Physiol 99(3):952–958 on Gymnacranthera canarica (King) Warb.—a Vulnerable tree
Grushvitzky IV (1967) After-ripening of seeds of primitive tribes of species of a highly threatened Myristica swamp ecosystem.
angiosperms, conditions and peculiarities. In: Physiologie, J Threat Taxa 8(7):9009–9013
Ökologie und Biochemie der Keimung, pp 329–336 Koilpillai YJ (2017) Ex situ conservation of the rare and endemic
Gutiérrez CL, Vovides A (1997) An in situ study of Magnolia species of Poeciloneuron pauciflorum bedd. World J Pharm Sci
dealbata Zucc. in Veracruz State: an endangered endemic tree of 6(12):1505–1509
Mexico. Biodiv Cons 6:89–97 Krishnapillay B, Mansor M, Yap SK, Chua LSL, Ang KC, Bakar
Gutiérrez-Nicolás F, Ravelo AG, Zárate R (2008) Seed germination SAA, Salleh Z (1991) Determination of seed testing standards–
and in vitro propagation of Maytenus canariens through moisture content of Hopea odorata seeds. J Trop For Sci
regeneration of adventitious shoots from axillary and apical 4(2):170–178
buds. Biol Plant 52(1):173–176 Kumar CA, Babu KP, Krishnan PN (2002) Seed storage and viability
Gutterman Y (1993) Seed germination in desert plants. Springer, of Myristica malabarica Lam. an endemic species of Southern
Berlin, p 253 Western Ghats (India). Seed Sci Technol 30(3):651–657
Han CY, Long CL (2010) Dormancy, germination and storage of Lamb FB (1966) Mahogany of tropical America: its ecology and
Magnolia ingrata seeds. Seed Sci Technol 38(1):252–256 management. University of Michigan, Ann Arbor
Han CY, Welbaum G, Long CL (2010) Seed dormancy and Lamont BB, Klinkhamer PG, Witkowski ETF (1993) Population
germination of Michelia yunnanensis (Magnoliaceae). Sci Hort fragmentation may reduce fertility to zero in Banksia goodii—a
124:3–87. https://doi.org/10.1016/j.scienta.2009.11.021 demonstration of the Allee effect. Oecologia 94:446–450
He YK, Xue WX, Sun YD, Yu XH, Liu PL (2000) Leafy head Lorente-Adame RG, Sánchez-Velásquez LR (1996) Dinámica esta-
formation of the progenies of transgenic plants of Chinese cional del banco de frutos del Teocintle Zea diploperennis
cabbage with exogenous auxin genes. Cell Res 10:151–602. (Gramineae). Biotropica 28:267–272
https://doi.org/10.1038/sj.cr.7290044 Luijten SH, Dierick A, Oostermeijer B, Raijmann LEL, Den Nijs
Hilaire RS (2001) Seed coat treatments influence germination of HCM (2000) Population size, genetic variation, and reproductive
Taxodium mucronatum. Desert Plants. http://hdl.handle.net/ success in a rapidly decling, self-incompatible perennial (Arnica
10150/554341 montana) in The Netherlands. Cons Biol 14(6):1776–1787
Hilhorst HWM, Bentsink L, Koornneef M (2006) Dormancy and Maku JO, Gbadamosi AE, Fadoju OA (2014) Germination and
germination. In: Basra AS (ed) Handbook of seed science and seedling growth of Mansonia altissima (A. Chev) in response to
technology. The Haworth Press, New York, pp 271–302

Author's personal copy
208 V. Iralu et al.

hormonal treatment. Intl J Agric For 4(4):269–274. https://doi. in a mixed conifer stand. New For 20:119–133
org/10.5923/j.ijaf.20140404.02 Öster M, Eriksson O (2007) Sex ratio mediated pollen limitation in
Mamani G, Chuquillanqui H, Chumbiauca S, Sahley C, Alonso A, the dioecious herb Antennaria dioica. Écoscience 14:387–398
Linares-Palomino R (2018) Substrate, moisture, temperature and Paal J (1998) Rare and threatened plant communities of Estonia. Biod
seed germination of the threatened endemic tree Eriotheca Cons 7:1027–1049
vargasii (Malvaceae). Rev Biol Trop 66(3):1162–1170 Padmalatha K, Prasad MNV (2007) Seed germination studies in
Martins JM, Moreira OCB, Rainha NFP, Baptista JAB, Silva L, Pterocarpus santalinus L.f.—an endandered and endemic
Moura MMT (2012) Morphophysiological dormancy and ger- medicinal plant, and relevance to conservation. Seed Sci
mination in seeds of the Azorean tree Picconia azorica. Seed Sci Biotechnol 1(2):32–34
Technol 40(2):163–176 Pan R, Sun W (2009) Seed dormancy and germination of the critically
McCleary BV, Matheson NK (1974) Galactomannan structure and b- endangered Manglietia grandis Hu et Cheng. Plant Physiol
mannanase and b-mannosidase activity in germinating legume Comm 45(11):1089–1092
seeds. Phytochem 14:1187–1194 Parry M, Parry ML, Canziani O, Palutikof J, Van der Linden P,
Meurk CD, Hall GMJ (2006) Options for enhancing forest biodiver- Hanson C (eds) (2007) Climate change 2007-impacts, adaptation
sity across New Zealand’s managed landscapes based on and vulnerability: working group II contribution to the fourth
ecosystem modelling and spatial design. N Z J Ecol assessment report of the IPCC, vol 4. Cambridge University
30(1):131–146 Press, Cambridge
Milberg P (1994) Germination ecology of the endangered grassland Pérez HE, Criley RA, Baskin CC (2008) Promoting germination in
biennial Gentianella campestris. Biol Cons 70:287–290 dormant seeds of Pritchardia remota (Kuntze) Beck., an
Morales P (1993) Deteccion e identificacion del insecto perforador endangered palm endemic to Hawaii. Nat Areas J 28(3):251–260
de semillas de Hualo (Nothofagus glauca (Phil.) (Krasser). Taller Petit RJ, Hampe A (2006) Some evolutionary consequences of being
de Habilitacion Profesional, Facultad de Ciencias Agrarias y a tree. Annu Rev Ecol Evol Syst 37:187–214
Forestales. Universidad Cato’-lica del Maule, Talca, Chile, p 31 Philippi T (1993) Bet-hedging germination of desert annuals:
Morandini MN, Giamminola EM, de Viana ML (2013) Desiccation variation among populations and maternal effects in Lepidium
tolerance in seeds of Prosopis ferox and Pterogyne nitens lasiocarpum. Am Nat 142:488–507
(Fabaceae). Rev Biol Trop 61(1):335–342. https://doi.org/10. Qaderi MM, Cavers PB (2000) Variation in germination response
15517/RBT.V61I1.11132 within Scotch thistle, Onopordum acanthium L., populations
Mukhia PK (2006) Management guidelines for Illicium griffithii for matured under greenhouse and field conditions. Ecoscience
community forests of Bhutan. PFMP Report 32. Social Forestry 7:57–65
Division, DoF, MoA Queenborough SA, Mazer SJ, Vamosi SM, Garwood NC, Valencia R,
Negash L (2004) Rapid seed-based propagation method for the Freckleton RP (2009) Seed mass, abundance and breeding
threatened African cherry (Prunus africana). New Forest system among tropical forest species: do dioecious species
27(3):215–227 exhibit compensatory reproduction or abundances? J Ecol
Negreros-Castillo P, Snook LK, Carl W, Mize CW (2003) Regen- 97:555–566
erating mahogany (Swietenia macrophylla) from seed in Quin- Raich JW, Khoon JW (1990) Effect of canopy openings on tree seed
tana Roo, Mexico: the effects of sowing method and clearing germination in a Malaysian dipterocarp forest. J Trop Ecol
treatments. For Ecol Manag 183:351–362 6:203–217
Ni WM, Chen XY, Xu ZH, Xue HW (2002) A Pin gene families Ramasubbu R, Irudhyaraj DF (2016) Reproductive biology of
encoding components of auxin efflux carriers in Brassica juncea. Elaeocarpus blascoi Weibel, an endemic and endangered tree
Cell Res 12(3–4):247–255 species of Palni Hills, Western Ghats, India. Curr Sci
Nikolaeva MG (1969) Physiology of deep dormancy in seeds. 110(2):234–240
Izdatel’stvo Nauka, Leningrad. Translated from Russian by Z. Renner SS (2014) The relative and absolute frequencies of
Shapiro. National Science Foundation, Washington, DC angiosperm sexual systems: dioecy, monoecy, gynodioecy, and
Nikolaeva MG (1977) Factors controlling the seed dormancy pattern. an updated online database. Am J Bot 101:1588–1596
In: Khan AA (ed) The physiology and biochemistry of seed Renner SS, Ricklefs RE (1995) Dioecy and its correlates in the
dormancy and germination. North Holland, Amsterdam, flowering plants. Am J Bot 82:596–606
pp 51–74 Reyes O, Casal M (2006) Seed germination of Quercus robur, Q.
Nilsson MC, Zackrisson O, Sterner O, Wallstedt A (2000) Charac- pyrenaica and Q. ilex and the effects of smoke, heat, ash and
terisation of the differential interference effects of two boreal charcoal. Ann For Sci 63(2):205–212
dwarf shrub species. Oecologia 123:122–128 Robbins AMJ (1988) Storage of champ (Michelia champaca) seed.
Nyman B (1963) Studies on the germination in seeds of Scots pine Banko Janakari 2:55–57
(Pinus sylvestris L) with special reference to the light factor. Rogers GM (1996) Regeneration ecology, conservation status and
Stud For Suecica 2:159 recovery planning for the endangered tree Olearia hectorii.
Nzekwe U, Ubani CS, Ajuziogu GC (2013) Effects of seed pre- Department of Conservation, Wellington, p 33
treatment and media on seed germination. Afr J Agric Res Rojas H (1996) Ciclo Biológico de Perzelia sp. en Hualo (Nothofagus
8(18):2057–2062 glauca (Phil.)(Krasser). Taller de Habilitación Profesional,
Ohya I, Nanami S, Itoh A (2017) Dioecious plants are more Facultad de Ciencias Agrarias y Forestales. Universidad Católica
precocious than cosexual plants: a comparative study of relative del Maule, Talca, p 31
sizes at the onset of sexual reproduction in woody species. Ecol Sanchez ML, Gurusinghe SH, Bradford KJ, Vazquez-Ramos JM
Evol 7(15):5660–5668 (2005) Differential response of PCNA and Cdk—a proteins and
Oldfield S, Lusty C, MacKinven A (1998) The world list of threatened associated kinase activities to benzyladenine and abscisic acid
trees. IUCN, WCMC, New York during maize seed germination. J Exp Bot 56(412):515–523.
Oleskog G, Sahlén K (2000) Effect of seedbed substrate on moisture https://doi.org/10.1093/jxb/eri029
conditions and germination of Scots pine (Pinus sylvestris) seeds

Author's personal copy
Ecology of seed germination in threatened trees: a review 209

Savithramma N, Ankanna S, Bhumi G (2012) Effect of nanoparticles Vary LB, Gillen DL, Randrianjanahary M, Lowry PPII, Sakai AK,
on seed germination and seedling growth of Boswellia ovalifo- Weller SG (2011) Dioecy, monoecy, and their ecological
liolata—an endemic and endangered medicinal tree taxon. Nano correlates in the littoral forest of Madagascar. Biotropica
Vision 2(1–3):61–68 43:582–590
Schlessman MA, Vary LB, Munzinger J, Lowry PP (2014) Incidence, Vásquez-Morales SG, Sánchez-Velásquez LR (2011) Seed ecology
correlates, and origins of dioecy in the island flora of New and pre-germinative treatments in Magnolia schiedeana Sch-
Caledonia. Int J Plant Sci 175:271–286 lecht, an endangered species from Mexico. J Food Agric Environ
Schmidt L, Jøker D (2000) Swietenia mahagoni (L.) Jacq. Seed 9(1):604–608
Leaflet-Danida Forest Seed Centre (18) Vazquez Yanes C, Perez Garcia B (1976) Notas sobre la morfologia y
Schütz W (2000) The importance of seed regeneration strategies for la anatomia de la testa de las semillas de Ochroma lagopus Sw
the persistence of species in the changing landscape of Central (Notes on the morphology and anatomy of the seed coat of
Europe. Z Ökol Nat 9:73–83 Ochroma lagopus Sw.). Turrialba 26(3):310–311
Scotland RW, Wortley AH (2004) How many species of seed plants Venier P, Ferreras AE, Verga A, Funes G (2015) Germination traits of
are there? Taxon 52(1):101–104 Prosopis alba from different provenances. Seed Sci Technol
Seppälä R, Buck A, Katila P (2009) Adaptation of forests and people 43(3):548–553
to climate change. IUFRO world series volume 22, Helsinki, Vijayan V, Rahees N (2015) Influence of light on seed germination of
p 224 sandal (Santalum album Linn.). BIOINFOLET Q J Life Sci
Sharma J, Graves WR (2004) Germination of Leitneria floridana 12(1c):278–279
seeds from disjunct populations. HortScience 39(7):1695–1699 Vovides A, Iglesias C (1996) Seed germination of Magnolia dealbata
Shu X, Yang Z, Duan H, Yang X, Yu H (2010) Seed germinating Zucc. (Magnoliaceae). An endangered species from Mexico.
characteristics of endangered plant Magnolia officinalis. China J HortScience 31:877
Chin Mater Med 35(4):419–422 Wang A, Wang X, Ren Y, Gong X, Bewley J (2005) Endo-b-
Simpson RL, Leck MA, Parker VT (1989) Seed banks: general mannanase and b-mannosidase activities in rice grains during
concepts and methodological issues. In: Leck MA, Thomas VT, and following germination, and the influence of gibberellin and
Simpson RL (eds) Ecology of soil seed banks. Academic, San abscisic acid. Seed Sci Res 15(3):219–227. https://doi.org/10.
Diego 1079/SSR2005212
Singh BG, Warrier RR, Anandalakshmi R, Sivakumar V, Sivalingam Whelan RJ (1995) The ecology of fire. Cambridge University Press,
R, Mahadevan NP, Chevanan G (2005) Seed germination studies Cambridge
in Saraca asoca (Roxb.) de Wilde. Indian For 131(6):841–843 Wood CB, Pritchard HW (2003) Germination characteristics of fresh
Sivakumar V, Warrier RR, Anandalakshmi R, Tigabu M, Odén PC, and dried Hyophorbe lagenicaulis seeds. Palms-Lawrence
Vijayachandran SN, Geetha S, Singh BG (2006) Germination 47(1):45–50
requirements and storage behavior of Myristica dactyloides Xia J, Lu J, Wang ZX, Hao BB, Wang HB, Liu GH (2013) Pollen
Gaertn. seeds. Seed Sci Technol 34:729–733 limitation and Allee effect related to population size and sex
Socolowski F, Takaki M (2004) Germination of Jacaranda mimosi- ratio in the endangered Ottelia acuminata (Hydrocharitaceae):
folia (D. Don–Bignoniaceae) seeds: effects of light, temperature implications for conservation and reintroduction. Plant Biol
and water stress. Braz Arch Biol Technol 47(5):785–792 15:376–383
Tabin T, Shrivastava K (2014) Factors affecting seed germination and Xiaohua S, Nianlin L, Ling J, Qiugui Z, Benmei X (1999) Seed
establishment of critically endangered Aquilaria malaccensis dormancy and germination of Sinojackia xylocarpa. J Zhejiang
(Thymelaeaceae). Asian J Plant Sci Res 4(6):41–46 For Coll 16(3):228–233
Thaman RR, Thomson LA, DeMeo R, Areki F, Elevitch CR (2006) Xiaojin JIN (2015) Effects of different illumination intensity and
Intsia bijuga (vesi). Species profiles for Pacific Island agro- moisture on seed germination of Parashorea chinensis. Agric
forestry. Permanent Agriculture Bogor-Indonesia Sci Technol 16(4):668–670
Thompson K, Bakker J, Bekker R (1997) The soil seed banks of North Yamaguchi S (2008) Gibberellin metabolism and its regulation. Annu
West Europe: methodology, density and longevity. Cambridge Rev Plant Biol 59:225–251
University, Cambridge Yang QH, Ye WH, Yin XJ (2007) Dormancy and germination of
Thompson K, Grime JP (1979) Seasonal variation in the soil seed Areca traindra seeds. Sci Hort 113:107–111
banks of herbaceous species in ten contrasting habitats. J Ecol Yildirim H, Özel ME, Akca A, Özdem M (2009) Observing the
67:893–921 effects or rapid industrialization, on forestry and pastures by
Tillberg E (1992) Effect of light on abscisic acid content in remote sensing. Allg. Forst-Jagdztg, p 151
photosensitive Scots pine (Pinus sylvestris L.) seed. Plant Youssef S, Lahcen O, Abdelaziz A (2012) Breaking seed dormancy in
Growth Regul 11:147–152 Cupressus atlantica Gaussen, an endemic and threatened conif-
Tompsett PB (1991) A review of the literature on storage of erous tree in Morocco. J For Res 23(3):385–390
dipterocarp seeds. BIOTROP Special Publication, Jakarta Yu Y, Baskin JM, Baskin CC, Tang Y, Cao M (2008) Ecology of seed
Upadhaya K, Barik SK, Adhikari D, Baishya R, Lakadong NJ (2009) germination of eight non-pioneer tree species from a tropical
Regeneration ecology and population status of a critically seasonal rain forest in southwest China. Plant Ecol 197:1–16
endangered and endemic tree species (Ilex khasiana Purk.) in Yuan RL, Xiang ZY, Yang WZ (2013) Seed dormancy and
North eastern India. J For Res 20:223–228 germination traits of Nyssa yunnanensis. For Res 26:384–388
Vamosi JC, Vamosi SM, Barrett SCH (2006) Sex in advertising: Zheng YL, Sun WB (2009) Seed germination of Huagaimu, a
dioecy alters the net benefits of attractiveness in Sagittaria critically endangered plant endemic to Southeastern Yunnan,
latifolia (Alismataceae). Proc R Soc B 273:2401–2407 China. Hort Technol 19(2):427–431
Van Daalen JC (1991) Germination of Pterocarpus angolensis seed. Zhou J, Kulkarni MG, Huang LQ, Guo LP, Van Staden J (2012)
Sh Afr For J 158(1):33–36 Effects of temperature, light, nutrients and smoke-water on seed
van Staden J, Brown NAC, Jäger AK, Johnson TA (2000) Smoke as a germination and seedling growth of Astragalus membranaceus,
germination cue. Plant Species Biol 15:167–178

Author's personal copy
210 V. Iralu et al.

Panax notoginseng and Magnolia officinalis—highly traded Visited websites

Chinese medicinal plants. S Afr J Bot 79:62–70
Zulueta-Rodrı́guez R, Soto M (1993) Bioclimatologı’a de Flora de http://www.dendrology.org/publications/tree-of-the-year/taiwania-
Veracruz. Magnoliaceae. Instituto de Ecologı́a, A.C. University cryptomerioides-2010/
of California, Riverside, CA. No. 6, México http://www.cpp.edu/*ejquestad/hawaiipropguide/Nothocestrum%20
Zulueta-Rodrı́guez R, Hernández-Montiel LG, Murillo-Amador B, breviflorum.html
Rueda-Puente EO, Capistrán LL, Troyo-Diéguez E, Córdoba- http://tropical.theferns.info/viewtropical.php?id=Sapindus?oahuensis
Matson MV (2015) Effect of hydropriming and biopriming on
seed germination and growth of two Mexican fir tree species in
danger of extinction. Forests 6:3109–3122