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Review / Revisión
SEED TRAITS AND GERMINATION IN THE CACTACEAE FAMILY: A REVIEW ACROSS THE
AMERICAS
RASGOS SEMINALES Y GERMINACIÓN EN LA FAMILIA CACTACEAE: UNA REVISIÓN EN LAS
AMÉRICAS
IDDUNIEL BARRIOS 1*, IDJORGE A. SÁNCHEZ2, IDJOEL FLORES3, IDENRIQUE JURADO4
1Jardín Botánico Nacional, Universidad de La Habana, Cuba.
2Instituto de Ecología y Sistemática, Ministerio de Ciencia, Tecnología y Medio Ambiente, Cuba.
3División de Ciencias Ambientales, Instituto Potosino de Investigación Científica y Tecnológica, AC. México.
4Facultad de Ciencias Forestales, Universidad Autónoma de Nuevo León, Linares, México
*Corresponding author: duniel.barrios@gmail.com
Abstract
Cactaceae is the fifth taxonomic group with the highest proportion of threatened species. One way to contribute to the
preservation of this family is to understand the processes that promote seed germination.
How common is dormancy and seed banks in Cactaceae? Are there general patterns in cacti germination response to temperature,
light, water, salinity, phytohormones, hydration/dehydration cycles, mechanical or chemical scarification?
A total of 333 studies on cactus germination with information on 409 taxa.
since 1939 to January 2020.
A search of scientific articles in Google Scholar was performed with the words Cactaceae, cacti and cactus, in combination with
various matters on germination in English, Spanish and Portuguese.
The main germination studies in cactus deal with photoblasticism (275 taxa), temperature (205 taxa) and seed longevity (142 taxa).
Other lines of study in cactus germination (e.g., desiccation tolerance, vivipary, phytohormones, mechanical or chemical scarification, in vitro
germination, hydration/dehydration cycles, water and saline stress, serotiny, storage in cold, high temperature tolerance and soil seed bank)
include between 14 and 65 taxa. Cacti have only physiological dormancy and optimal germination for most species occur between 20 and
30 °C.
Mexico, Brazil and Argentina are the three leading countries in the study of cactus germination.
Dormancy, photoblasticism, seed bank, serotiny, temperature, viviparity.
Resumen:
Cactaceae constituye el quinto grupo taxonómico con mayor proporción de especies amenazadas. Uno de los aspectos que
contribuyen a la preservación de estas especies es el entendimiento de los procesos que promueven la germinación de sus semillas.
¿Qué tan común es la latencia y los bancos de semillas en Cactaceae?¿Existen patrones generales en la respuesta germinativa de
los cactus ante la temperatura, luz, agua, salinidad, fitohormonas, ciclos de hidratación/deshidratación o escarificación mecánica o química?
Se revisaron 333 estudios sobre germinación de cactus con información de 409 taxa.
Estudios de germinación de cactáceas en América, publicados desde 1939 a enero de 2020.
Se realizó una búsqueda de artículos científicos en Google Académico con las palabras Cactaceae y cactus, en combinación con
varias materias sobre germinación en inglés, español y portugués.
Los principales estudios sobre la germinación de cactáceas han versado sobre el fotoblastismo (275 taxones), la temperatura
(205 taxones) y la longevidad seminal (142 taxones). Otras líneas de estudio que abordan la germinación de cactus (e.g., tolerancia a la
desecación, viviparidad, fitohormonas, escarificación mecánica o química, germinación in vitro, ciclos de hidratación/deshidratación, estrés
hídrico y salino, serotinia, tolerancia a altas temperaturas y almacenamiento en frío, bancos de semillas) comprenden entre 14 y 65 taxones.
Las cactáceas presentan solo latencia fisiológica y una temperatura óptima de germinación entre los 20 y 30 °C.
México, Brasil y Argentina son los tres países líderes en el estudio de la germinación en cactus.
Banco de semillas, fotoblastismo, latencia, serotinia, temperatura, viviparidad.
Background:
Questions:
Data description:
Study site and dates:
Methods:
Results:
Conclusions:
Keywords:
Antecedentes:
Preguntas:
Descripción de datos:
Sitio y años de estudio:
Métodos:
Resultados:
Conclusiones:
Palabras claves:
Botanical Sciences 98(3): 417-440. 2020 Received: November 12, 2019, Accepted: March 19, 2020
DOI: 10.17129/botsci.2501 On line first: July 24, 2020
________________
This is an open access article distributed under the terms of the Creative Commons Attribution License CCBY-NC (4.0) international.
https://creativecommons.org/licenses/by-nc/4.0/
417
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Cactaceae is the family considered to have the largest
number of genera within the order Caryophyllales
(Hernández-Ledesma et al. 2015) and its species occupy a
wide range of habitats through the American continent
(Anderson 2001, Goettsch et al. 2015). For centuries cacti
have fascinated humans because of the beauty and the rarity
of the majority of their species (Bravo-Hollis 1978, Griffith
2004). Although the most widespread use is ornamental
(Goettsch et al. 2015), in several countries the fruits,
flowers and stems of 154 species are widely consumed
(Anderson 2001, Goettsch et al. 2015). Plants of the
Cactaceae are currently among the most vulnerable to
human disturbance because of their slow growth (Godínez-
Álvarez et al. 2003) and constitute the fifth taxonomic
group with the highest proportion of species threatened
worldwide (Goettsch et al. 2015).
One way to help preserve these species and others with
special conservation value is to understand the processes
that promote seed germination (Rojas-Aréchiga & Vázquez-
Yanes 2000, Anderson 2001, Flores et al. 2006). Two
remarkable works about cactus seeds have been published.
Rojas-Aréchiga & Vázquez-Yanes (2000) published an
exhaustive review on cactus seed germination. Barthlott &
Hunt (2000) published a book on cactus seed
micromorphology, including 213 species and
688 microphotographs from more than 350 taxa. In
addition, it contains the compilation of studies with
microphotographs of cactus seeds from 1,050 species of
230 genera (Rojas-Aréchiga 2012). Barthlott & Hunt (2000)
study describes 26 useful seed traits and attempts to
homogenize English terminology. Both Rojas-Aréchiga &
Vázquez-Yanes (2000) and Barthlott & Hunt (2000) studies
have been referenced for all research in cactus seed
germination and seed description during the last two
decades.
Since the 2000s, the papers on cactus seed germination
almost tripled the available information. This review aims
to perform an analysis of the cactus seed literature in the
last 80 years. The trends found and gaps in the information
are discussed. Specifically, we analyzed the relationship
between cactus seed germination and seed traits, as well as
between cactus seed germination and phylogeny. We also
documented the germination types in cacti, and how
common is seed dormancy and how common are seed banks
in the cactus family. We also discuss the effect of
temperatures, light, water, salt and hydration-dehydration
cycles on cactus seed germination.
Materials and methods
A search of scientific articles was performed with the
words Cactaceae, cacti or cactus in combination with:
germination, photoblasticism, seed bank, vivipary,
dormancy, hydration-dehydration cycle, serotiny and in
vitro germination through the search engine Google Scholar
(https://scholar.google.com), in English, Spanish, and
Portuguese, the main languages in the American continent.
According to Haddaway et al. (2015) Google Scholar is a
powerful tool for finding specific literature and is adequate
for identifying the majority of evidence in a systematic
review, the references from each study found were also
analyzed. In total 333 studies related to cactus germination
from 1939 to January 2020 (Figure 1, Tables 1 and 2) were
gathered, with information on 409 taxa. Cactus seed
germination has been evaluated in less than 50 % of the
genera. The collected information was grouped by subjects
and then discussed.
Figure 1. Number of studies of cactus seed germination until
January, 2020.
All the information obtained was divided into ten
subjects according topics covered in Baskin & Baskin
(2014) and that there were also several studies on cacti. In
the section on Cactus seed traits; shape, color, size, mass, as
well as appendices and number of seeds per fruit were
considered. The intention of this topic was to introduce
readers to the generalities of cactus seeds as a necessary
process to discuss the different issues related to
germination. Also the section on Germination types, that
relates the shape of the seed to the mode of germination,
was mainly considered as introductory. The information
discussed in these two subjects was obtained mainly from
classical or compilation studies (e.g., Flores & Engleman
1976, Bregman & Bouman 1983, Barthlott & Hunt 2000,
Rojas-Aréchiga & Vázquez-Yanes 2000, Seal et al. 2009).
The number of taxa studied by genera, subfamilies and
country or region of origin of the taxon was compiled for
the rest of the subjects. Seed dormancy, was not included in
the summary table because we used the number of cactus
species having seed dormancy from Willis et al. (2014). The
species where viviparity has been studied were also
included in the summary table.
Seed traits and germination in the Cactaceae
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In the subject Temperature and seed germination, the
mean and the confidence intervals of the germination
percentage at 30 °C were plotted between cacti from
temperate and warm climates. The type of weather was
obtained from the information of each article reviewed; the
comparison was based on 43 data from temperate and
34 from warm climate. Similarly, in the subject Water and
saline stress and germination, the mean and standard
deviation of the germination response of cactus seeds were
plotted against different water potentials induced with
polyethylene glycol (PEG).
On the subject Light and seed germination, we consider
the photoblastic response of the seeds according to the
Relative Light Germination index (RLG) (Milberg et al.
2000) and the proportions proposed by Funes et al. (2009).
Values with RLG > 0.75 were considered positive
photoblastic, < 0.25 negative photoblastic, species with
RLG values between 0.25 and 0.75 were considered
indifferent photoblastic (Funes et al. 2009). We calculate
the RLG, to define the photoblastic response of the seeds in
the studies where they had not calculated it.
Results and Discussion
Cactus seed traits. Both the works of Flores & Engleman
(1976) and Bregman & Bouman (1983), as well as of
Barthlott & Hunt (2000), present the structure and general
anatomy of cacti seeds. In such studies, it was shown that in
cacti the embryo is covered by two layers of tissue: the
external (known as the testa) is generally thick, while the
Table 1. Abstract of the cactus studies on different research lines related with seed germination in 80 years and 333 papers with information
on 409 taxa. Taxa: Number of taxa studied; Cact: Cactoideae; Opt: Opuntioideae; Per: Pereskioideae; Mah: Maihuenioideae. Countries or
regions, MX: Mexico; BR: Brazil; AR: Argentina; CH: Chile; PE: Peru; BO: Bolivia; PA: Paraguay; CO: Colombia; USA: Unites States of
America; CA: Caribbean region; SOU: South America; MX-U: Mexico - USA; CU: Cuba. It is possible to find a higher number of species per
country when in a same taxon several studies in natural populations from different countries were done. In parenthesis the percentage of
genera with at least one species studied.
Matter Genus Taxa Subfamilies Countries or regions
Cact Opt Per Mah MX BR AR CH PE BO PA CO USA CA SOU* MX-U* CU*
Photoblasticism 62 (50.0) 275 251 20 3 1 129 46 41 37 9 0 0 0 7 4 0 0 16
Temperatures 62 (50.0) 205 184 17 3 1 64 43 30 14 12 4 1 0 14 10 13 0 17
Longevity 143 (34.7) 142 128 12 1 1 70 25 10 19 2 1 0 0 11 2 7 0 9
Desecation tolerance 30 (24.2) 65 53 2 0 0 19 0 6 13 6 1 0 0 1 2 10 7 0
Vivipary 21 (16.9) 58 58 0 0 0 12 5 27 0 0 1 0 0 1 6 6 0 13
Phytohormones (AG3) 29 (23.4) 59 50 9 0 0 36 4 4 4 0 0 1 0 6 2 4 0 10
Mechanical or chemical
scarification 223 (18.5) 52 41 11 0 0 40 2 2 0 0 0 0 0 7 0 1 0 12
In vitro germination 18 (14.5) 42 38 4 0 0 26 14 0 0 0 0 0 0 0 3 0 0 0
Water stress 23 (18.5) 39 37 1 1 0 15 10 9 2 0 0 0 3 0 0 0 0 9
Serotiny 9 (7.2) 24 22 2 0 0 20 0 0 0 0 0 0 0 3 1 0 0 1
Hydration/dehydration cycles 11 (8.8) 20 20 0 0 0 11 2 7 0 0 0 0 0 0 0 0 0 1
Storage in cold 37 (5.6) 20 20 0 0 0 2 16 0 0 0 0 0 0 2 0 0 0 0
Soil seed bank 10 (8.1) 19 17 2 0 0 7 3 6 0 0 0 0 0 3 0 0 0 9
High temperature tolerance 9 (7.2) 17 13 4 0 0 14 1 0 0 0 0 0 0 3 0 0 0 0
Saline stress 8 (6.4) 14 12 2 0 0 7 7 0 0 0 0 0 0 0 0 0 0 8
1 It includes studies where the viability of seeds of at least three months stored at room temperature was tested.
2 It includes studies where the germination response was tested after subjecting the seeds to various scarification methods that include sand,
sandpaper, cuts (mechanical scarification) or with H2SO4, HCl, NaClO and H2O2 (chemical scarification).
3 Only studies where the seeds were kept at temperatures equal to or below 0 °C were included.
* The species referred for SOUD and MX-U comprise species where the seed collection site was not declared and the distribution covers two
or more countries. The references for Cuba were not added to the total species, because they include studies that have not yet been published,
the germination studies of Cuban cacti that have already been published were included in the Caribbean list.
Barrios et al. / Botanical Sciences 98(3): 417-440. 2020
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internal one only forms a fine membrane around the embryo
(Bregman & Bouman 1983) that completely collapses
during seed maturation in most species (Barthlott & Hunt
2000) (Figure 2). A distinctive trait in Cactaceae seeds, but
not exclusive of the family, is a small area called the hilum-
micropylar region, which is caused by the presence of
campylotropous ovules (Bregman & Bouman 1983,
Barthlott & Hunt 1993), although Flores & Engleman
(1976) considered the amphitropous ovules dominant. This
characteristic is considered a variant of campylotropous
ovules according to Font Quer (1973). For descriptive
purposes Barthlott & Hunt (2000) divided cactus seeds in
four regions: ventral, dorsal, apical and the edge of the
hilum-micropylar region.
Cactaceae seeds vary in shape. Bregman & Bouman
(1983) in their review presented 12 seed variants, while
Barthlott & Hunt (2000) in accordance with the treatment of
Voit (1979) considered eight types of seeds, which they
themselves reduced to four, according to the length/width
relationship. In general, cactus seeds have been described as
reniform, pyriform, globular, oval, hat-shaped, lenticular or
mussel-shaped (Rojas-Aréchiga & Vázquez-Yanes 2000,
Barthlott & Hunt 2000) (Figure 3). In spite of the great
variability of terminologies, the majority of the previous
studies have followed Barthlott & Hunt (2000) (see: Arias
& Terrazas 2004, Arroyo-Consultchi et al. 2006, 2007,
Arias et al. 2012, and Franco-Estrada et al. 2014). Although
it is possible that some relationship between the shape of
the cactus seeds and their germination exists, this aspect has
been little studied. Bregman & Bouman (1983) associated
the seed shape with differences in the formation of
germination cracks. Hat-shaped seeds occur in North
American genera such as Astrophytum and Epithelanta, as
well in species of several South American genera, such as
Frailea, Matucana, Discocactus, Notocactus (Parodia), and
Thrixanthocereus (Espostoa) (Barthlott & Hunt 2000).
Table 2. Taxa of the Cactaceae having at least nine species with seed germination studies. Taxonomy was based in Hunt et al. (2006).
Spp = Species number per genus. Review based in 333 papers published in the last 80 years.
Subfamily/genus spp With information Subfamily/Genus spp With information
Cactoideae Cactoideae
Armatocereus 9 1 Melocactus 50 18
Browningia 9 0 Micranthocereus 10 2
Cereus 29 6 Pachycereus 13 6
Cleistocactus 48 5 Parodia 66 8
Coleocephalocereus 10 1 Pediocactus 10 0
Copiapoa 30 6 Peniocereus 20 2
Corryocactus 12 1 Pfeiffera 10 0
Coryphantha 53 9 Pilosocereus 49 18
Discocactus 12 3 Pseudorhipsalis 9 0
Disocactus 16 1 Rebutia 40 1
Echinocereus 106 4 Rhipsalis 48 9
Echinopsis 101 28 Sclerocactus 28 2
Epiphyllum 18 4 Selenicereus 27 1
Eriosyce 51 17 Stenocereus 25 9
Escobaria 23 5 Thelocactus 20 3
Espostoa 12 2 Turbinicarpus 36 22
Ferocactus 42 13 Weberocereus 10 1
Frailea 18 1 Opuntioideae
Gymnocalycium 63 9 Austrocylindropuntia 9 0
Haageocereus 14 5 Corynopuntia 14 0
Harrisia 9 7 Cylindropuntia 33 5
Hylocereus 14 7 Opuntia 75 17
Leptocereus 11 1 Pterocactus 9 1
Mammillaria 232 43 Pereskioideae
Matucana 21 0 Pereskia 18 3
Seed traits and germination in the Cactaceae
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Experimental evidence of floating capabilities (hat shape, a
funicular envelope covering a prominent hilum, and air
chambers throughout the tegument) and potential water
dispersal of hat-shaped seeds in Cactaceae have been found
in Astrophytum capricorne and Astrophytum ornatum
(Sánchez-Salas et al. 2012), as well as in Astrophytum
myriostigma (Romero-Méndez et al. 2018). Seeds of
Selenicereus wittii from the Amazonia, in Brasil, are
mussel-shaped, and also have an air chamber and are
adapted to inundation hydrochory (Barthlott et al. 1997).
Figure 2. Transversal section of a cactus seed. t: testa; il: internal
layer and e: embryo. Drawing by Alfredo Ruiz Fleitas
Unlike the high variability in terms of shape, seed color
in the family is mainly between black and brown
(Leuenberger 1986, Barthlott & Hunt 2000, Arias &
Terrazas 2004, Arroyo-Consultchi et al. 2006, Seal et al.
2009, Arias et al. 2012, Loza-Cornejo et al. 2012, Franco-
Estrada et al. 2014). In some cases; however, they can be
reddish-brown, yellow, green or off-white (Rojas-Aréchiga
& Vázquez-Yanes 2000, Barthlott & Hunt 2000, Arias et al.
2012). A potential relationship between seed color and seed
germination in cactus remains to be tested.
Consistent with seed shape, the embryo of the cactus is
generally curved (Barthlott & Hunt 2000) and peripheral
(Finch-Savage & Leubner-Metzger 2006), with great
variation in the region that occupies the storage structure. In
Leuenbergeria, Opuntia and Pereskiopsis species, a greater
development of the cotyledons is observed with respect to
the hypocotyl. Nevertheless, the tendency in the family is a
greater development of the hypocotyl with respect to the
cotyledons. Cactus genera like Mammillaria and Parodia
show upright embryos with 90 % of the volume occupied
by the hypocotyl (Barthlott & Hunt 2000).
In terms of the average number of seeds produced per
fruit, an enormous variation exists in cacti. Some authors
report cactus fruits (e.g. Epiphyllum anguliger, Ferocactus
histrix, Pachycereus pringlei, P. weberi, Pilosocereus
chrysacanthus, Echinopsis atacamensis subsp. pasacana,
Gymnocalycium monvillei), with ranges between 1,000 and
8,000 seeds (Zimmer 1966, Del Castillo 1988, Fleming et
al. 1994, Valiente-Banuet et al. 1997, de Viana 1999,
Gurvich et al. 2008), although it is possible to find species
with fewer than 20 seeds per fruit in genera such as
Mammillaria (Valverde & Zavala-Hurtado 2006, Valverde
et al. 2015), Pereskia and Leuenbergeria (Leuenberger
1986).
Cactus seeds are generally smaller than one centimeter
(Barthlott & Hunt 2000, Seal et al. 2009, Rojas-Aréchiga et
al. 2013) and vary from 0.2 mm in Blossfeldia liliputana
(Barthlott & Porembski 1996) to 7.5 mm in Pereskia bleo
(Leuenberger 1986), and their weight varies from 0.016 mg
in Mammillaria bocasana (Flores et al. 2006) to 56.04 mg
in Opuntia basilaris (Royal Botanic Gardens Kew 2019).
Differences in seed mass among cactus species and
localities have been found, e.g., Romo-Campos et al. (2010)
found that Opuntia spp. seeds collected in moist areas were
heavier than those collected in dry sites. These authors also
found a correlation between seed mass and seed
germination for Opuntia jaliscana in which larger seeds
germinated more than smaller seeds. Sosa-Pivatto et al.
(2014) found no correlation between seed mass and
germination characteristics in central Argentinian cacti;
however, they found that species with heavier seeds
produced bigger and more cylindrical seedlings.
Other traits associated with cactus seeds are appendages
or structures, such as funicula, arils, strophioles and
mucilage. In the subfamily Opuntioideae, the ovule is
surrounded by the funiculus that is lignified during
development (Bregman & Bouman 1983, Strittmatter et al.
2002) and forms a structure considered as an aril by
Barthlott & Hunt (2000) but as a covering by Bravo-Hollis
(1978). Orozco-Segovia et al. (2007) found that lignified
funiculus in Opuntia tomentosa acts as a partial barrier to
water diffusion into the seed and that in this species, water
uptake occurs mainly through the water channel mediated
by a valve, both formed in the hilum-micropyle region
during seed dehydration and ageing. Various genera like
Mammillaria, Aztekium (Bravo-Hollis 1978) and
Blossfeldia (Barthlott & Hunt 2000) show strophioles that
can be considered arils, but to differentiate them from the
structure of Opuntioideae, this term has continued to be
used (Barthlott & Hunt 2000). A mucilage sheath is present
in more than 40 species of cactus belonging to 22 genera
and is formed by pectins (Barrios et al. 2015, Mascot-
Gómez et al. 2020). Bregman & Graven (1997) and
Mascot-Gómez et al. (2020) suggested that the layer of
mucilage in cactus seeds improves the germination through
the effect of the intake and distribution of water. Barrios et
al. (2015) suggested that maybe the presence of mucilage in
Barrios et al. / Botanical Sciences 98(3): 417-440. 2020
421
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Leptocereus scopulophilus seeds serves other purposes such
as the adhesion of seeds to the soil or camouflage from seed
eaters.
Germination types. Seed germination is a series of events
that begin with imbibition and end with the emergence of
the radicle from the seed coat. There are few studies that
consider germination types in Cactaceae (Almeida et al.
2009, Secorun & Souza 2011), since the classic study by
Bregman & Bouman (1983). The aforementioned authors
described 11 variants of germination where the radicle is the
first organ of the seedling to break the testa and
hypothesized the phylogenetic relationships between
variants. In addition, they considered that the mode of
germination in a cactus is correlated to the seed shape, and
they defined the Cereus variant as the most numerous in the
family. Curiously, although for the genus Leptocereus
Areces-Mallea (2003) only recognized the Cereus variant in
two species (L. quadricostatus and L. sylvestris), García-
Beltrán et al. (2017) found four variants in only one species
(L. scopulophilus). In addition to the Cereus variant in L.
scopulophilus, García-Beltrán et al. (2017) recognized the
Pereskia variant and another two where the cotyledons are
the first organ to break the testa. The aforementioned
variants were considered exceptions by Bregman &
Bouman (1983). Nevertheless, in one of the seed morphs of
L. scopulophilus, these “alternative variants” account for
over 20 % (García-Beltrán et al. 2017).
Seed dormancy. Rojas-Aréchiga & Vázquez-Yanes (2000)
only found reports of seeds with innate and forced
dormancy. The forced dormancy of seeds is considered by
Baskin & Baskin (2014) as non-dormant. The classification
proposed by those authors establishes that seeds that
germinate within the first four weeks after dispersion are
non-dormant and that the seeds that do not germinate
because of inadequate conditions (forced dormancy) must
be considered as latent or quiescent. Previous cactus studies
have reported viviparous seeds (without innate dormancy)
in 58 species (Table 1) (Cota-Sánchez 2004, Cota-Sánchez
et al. 2007, 2011, Rojas-Aréchiga & Mandujano-Sánchez
2009, Barrios et al. 2012, Aragón-Gastélum et al. 2013,
2017). Viviparous are also considered as non-dormant in the
system of Baskin & Baskin (2014). The studies about cactus
Figure 3. Shape of cactus seeds. A: globular (Blossfeldia liliputana); B: lenticular (Leuenbergeria bleo); C: pyriform (Escobaria cubensis); D:
mussel-shaped (Selenicereus grandiflorus); E: reniform (Neobuxbaumia multiareolata); F: hat-shaped (Frailea phaeodisca). According
Barthlott & Hunt (2000) A and B: circular; C and D: oval; E and F: broadly oval. Drawings by Alfredo Ruiz Fleitas
Seed traits and germination in the Cactaceae
422
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seed dormancy are few (Potter et al. 1984, Côrtes et al.
1994, Olvera-Carrillo et al. 2003, Mandujano et al. 2005,
Flores et al. 2005, 2008, Orozco-Segovia et al. 2007,
Delgado-Sánchez et al. 2010, 2011, 2013), may be because
of the rapid germination that the majority of the studied
species possess. In addition, few works about germination
mention how many un-germinated seeds are dormant
(Flores et al. 2005, 2006, Ortega-Baes et al. 2010, Aragón
& Lasso 2018).
The most used methods for interrupting dormancy in
cactus seeds have been through chemical scarification (by
immersion in H2SO4, HCl, NaClO and H2O2 at various
concentrations and times) and mechanical scarification,
which together encompass some 52 species studied
(Table 1). In addition, gibberellic acid has been used as a
promoter of germination, but its role is discussed later in
reference to light. Few studies have used thermal shock but
without obtaining good results with this type of treatment
(Sánchez-Venegas 1997, Rosas-López & Collazo-
Ortega2004, Carbajal et al. 2010, Villanueva et al. 2016,
Podda et al. 2017, Gonzalez-Cortés et al. 2018). Other
studies have used fungal inoculation in some species of
Opuntia (Delgado-Sánchez et al. 2010, 2011, 2013) or
hydration/dehydration cycles (Dubrovsky 1996, 1998,
Santini & Martorell 2013, Contreras-Quiroz et al. 2016a,
2016b) with good results. Research in the last decade that
has addressed treatments to break dormancy in cactus seeds
are however, not common (Rojas-Aréchiga et al. 2011,
Amador-Alférez et al. 2013, Delgado-Sánchez et al. 2010,
2011, 2013, Podda et al. 2017, Gonzalez-Cortés et al.
2018).
In cacti, a rapid and high percentage of germination is
associated with a thin testa (Maiti et al. 1994). However,
although testa functions as regulator in imbibition (Souza &
Marcos-Filho 2001), physical dormancy has not been found
in cactus seeds. Although works about germination in
Opuntia and Harrisia have suggested the presence of
physical, morphological or morphophysical dormancy
(Potter et al. 1984, Olvera-Carrillo et al. 2003, Podda et al.
2017), morphological (Mandujano et al. 1997) or
morphophysiological (Dehan & Pérez 2005). None of these
studies demonstrated a lack of seed imbibition, or an
undifferentiated or underdeveloped embryo, which are traits
used to show the existence of these types of dormancy
(Baskin & Baskin 2014). Previous studies of Opuntia
(including the species erroneously classified with physical
and morphological dormancy) have demonstrated that only
physiological dormancy can be attributed to them
(Mandujano et al. 2005, Orozco-Segovia et al. 2007). In
addition, cactus seeds having physiological dormancy can
show dormancy cycling, Aragón-Gastélum et al. (2018)
found that buried seeds of Echinocactus platyacanthus
acquired secondary dormancy in the rainy seasons (summer
and autumn), which was alleviated at the end of the
subsequent dry season (winter), possibly because of the
high variation registered in mean and minimum soil
temperature at the end of winter.
Finch-Savage & Leubner-Metzger (2006), Willis et al.
(2014) and Baskin & Baskin (2014) currently only
recognize non-dormant seeds (including viviparous) and
seeds with physiological dormancy for Cactaceae.
According to Willis et al. (2014), in 153 cactus species
studied 65 % showed physiological dormancy and 35 %
non-dormant seeds. Most cacti inhabit arid and semiarid
environments, so it is expected that future studies will find
new species with physiological dormancy and probably
species with physical dormancy as an adaptation to delay of
germination, as has been proposed for species that occupy
extreme or seasonal habitats (Jurado & Flores 2005, Baskin
& Baskin 2014). In addition, a greater presence of
heteromorphism in Cactaceae seeds with different degrees
of physiological dormancy could be expected, as it occurs
in Leptocereus scopulophilus (García-Beltrán et al. 2017)
and Leptocereus arboreus seeds (unpublished data). Seed
heteromorphism is considered a “bet hedging” strategy that
favors the reproductive success of the offspring in
unpredictable and heterogeneous environments (Venable
2007).
Seed banks. A seed bank is formed through the presence of
viable seeds that remain in the habitat without germinating
during a given period (Thompson & Grime 1979). Two
types of banks have been defined in terms of the longevity
of the seeds: a transient seed bank, when the seeds do not
stay viable for more than a year (Thompson & Grime 1979)
or until the next germination season (Walck et al. 2005) and
a persistent seed bank when the seeds achieve permanence
for more than a year.
When the place where the seeds are stored is referred to,
two types of banks have been described: aerial and
terrestrial (Baskin & Baskin 2014). Seeds are typically
stored in the soil (the soil or terrestrial seed bank) but, in
some species, seeds may be retained in plant canopy (the
aerial seed bank) until seed release is triggered (Günster
1992). The formation of seed banks requires from the
species an orthodox storage behavior that allows them to
remain viable for long periods, as well as to escape from
predators (Baskin & Baskin 2014).
The first studies about cactus seed banks concluded their
existence whether through the collection of viable seeds in
the soil (de Viana 1999), by examining seeds viability after
different burial periods (Bowers 2000, 2005) or the
dormancy present in some species (Potter et al. 1984,
Mandujano et al. 1997). Silvius (1995) observed that
Stenocereus griseus seeds obtained from bird feces took
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between two and five months to germinate, so at least a
transient seed bank was possible for the species.
Most of the cactus seeds studied show small size, positive
photoblasticism or skotodormancy (seed dormancy after
darkness incubation) that allow them to persist in seed
banks (Rojas-Aréchiga & Vázquez-Yanes 2000, Rojas-
Aréchiga & Batis 2001, Flores et al. 2006, 2011, Ruiz-
González et al. 2011, Rojas-Aréchiga et al. 2013, Sosa-
Pivatto et al. 2014, Bauk et al. 2017, García-Beltrán et al.
2017, Rojas-Aréchiga & Mandujano-Sánchez 2017).
Corresponding to the expected behavior for such seed traits,
Seal et al. (2009) published a database with 83 species with
seeds that remained viable for more than a year after
collection and 65 species with desiccation tolerance. We
found one hundred and forty-two cacti species contain seeds
capable of remaining viable for at least three months after
collection (Table 1). Even some works where the cactus
seeds were stored under controlled conditions have
demonstrated that these can germinate after various years
(Flores et al. 2005, Sánchez-Salas et al. 2006) up to a
maximum of 10 years (Alcorn & Martin 1974, Fearn 1977,
Trujillo et al. 2014). Few studies have directed their efforts
toward evaluating the viability of cactus seeds under natural
conditions and their permanence in seed banks (Álvarez-
Espino et al. 2014, Aragón-Gastélum et al. 2018).
Some recent work suggests the possibility of seed banks
because of germination trials for various months or years
(Flores et al. 2005, Faife-Cabrera & Toledo-Reina 2007, De
la Rosa-Manzano & Briones 2010, Salazar et al. 2013,
Jiménez-Sierra & Matías-Palafox 2015) or through the
collection and measurement of seed viability (Cano-Salgado
et al. 2012), although in this case it is impossible to
determine the age of the collected seeds. Only in 19 species
has the existence of a seed bank in the soil been clearly
established (Table 1).
There are few studies that have submitted the seeds to
environmental conditions and have examined their viability
after different burial periods (Bowers 2000, 2005, Matías-
Palafox 2007 Olvera-Carrillo et al. 2009, Cheib & Souza
2012, Goodman et al. 2012, Álvarez-Espino et al. 2014,
Ordoñez-Salanueva et al. 2017, Lindow-López et al. 2018a,
Aragón-Gastélum et al. 2018) or have assessed the effective
seed bank, extracting the seeds from the soil in different
times of the year (Montiel & Montaña 2003). Only the
studies of Bowers (2005) and Ordoñez-Salanueva et al.
(2017) shows two species (Mammillaria grahamii and
Polaskia chende) capable of possessing a long-term,
continuous seed bank (up to at least five years) according to
the classification of Bakker et al. (1996).
Serotiny represents an alternative to the traditional seed
bank and in many cases is known as an aerial form of seed
bank, with the advantage of protecting the seeds in
structures that are inaccessible to predators (Rodríguez-
Ortega et al. 2006). Serotiny is known as a delayed
dispersion mechanism because of the retention of mature
seeds in structures of the mother plant for more than a year
(Peters et al. 2009). In the Cactaceae family, serotiny
probably is a common phenomenon in species that inhabit
several North American deserts like the Mojave and the
Sonora (Martínez-Berdeja et al. 2015). So far 24 species of
cacti with a retention of mature seeds have been listed
(Table 1), although around 25 species showed some degree
of retention in the work of Bravo-Hollis & Sánchez-
Mejorada (1991) according to Peters et al. (2009) but the
role that serotiny plays in the population dynamic of the
species where it occurs has not been extensively studied.
Seed retention in cacti has been observed in the axils of
tubers (Rodríguez-Ortega et al. 2006, Peters et al. 2009), in
chained fruits (Martínez-Berdeja et al. 2015), in the apex of
the stems and in the cephalia (Bravo-Hollis & Sanchez-
Mejorana 1991). The duration of the seeds in the stems has
mainly been studied in the Mammillaria genus, where it has
been demonstrated that the seeds can be retained from one
(Santini & Martorell 2013) to eight years, forming an aerial
seed bank (Boke 1960, Peters et al. 2009, Rodríguez-Ortega
et al. 2006).
Temperature and seed germination. The current knowledge
about the germination response of cactus seeds concerning
different temperatures includes approximately 205 taxa
(Table 1); the majority possesses an optimal germination
between 20 - 30 °C (Zimmer 1968, 1982, 1998, Rojas-
Aréchiga & Vázquez-Yanes 2000, Meiado et al. 2016, Seal
et al. 2017). In a few species, greater germination was
obtained at 15 °C, including those found in Parodia
aureicentra, Pereskia grandifolia subsp. grandifolia,
Pereskia bahiensis, Pereskia aculeata, Echinopsis
schickendantzii, Acanthocalycium spiniflorum, Ferocactus
glaucescens, Mammillaria polythele, Browningia
hertlingiana, Cephalocereus senilis, Rebutia minuscula,
Rhipsalis pilocarpa, Rhipsalis teres and Copiapoa cinerea
var. haseltoniana (Zimmer 1968, 1982, 1998, Ortega-Baes
et al. 2011, Lone et al. 2016, Meiado et al. 2016, Seal et al.
2017, Lindow-López et al. 2018b). Most of the species
mentioned above inhabit temperate climates with annual
average temperatures between 10.1 and 19.4 °C (https://
es.climate-data.org), except Pereskia spp. and Rhipsalis spp.
that inhabit warm climates with annual averages between
23.2 and 26.4 °C (Da Silva 2004, https://es.climate-
data.org).
There are species with different growth forms with seeds
that can germinate more than 50 % at temperatures as high
as 40 °C. The majority have been reported in columnar
species such as: Pilosocereus gounellei subsp. gounellei,
Pilosocereus pachycladus subsp. pernambucoensis (Meiado
et al. 2016), Stenocereus thurberi, Pachycereus pringlei,
Seed traits and germination in the Cactaceae
424
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Pachycereus pecten-aboriginum, Ferocactus peninsulae
(Yang et al. 2003) and Stenocereus griseus (Arias &
Williams 1978), as well as the globular species Melocactus
curvispinus subsp. caesius (Arias & Lemus 1984) and the
epiphyte Selenicereus setaceus (Simão et al. 2007). The
general tendency however, in cacti is that temperatures
equal or higher than 35 °C and lower than 15 °C do not
promote germination (Zimmer 1968, 1982, 1998, Rojas-
Aréchiga & Vázquez-Yanes 2000, Meiado et al. 2016, Seal
et al. 2017).
Because temperatures continually vary in nature, various
studies have compared the germination response of the
cactus seeds between constant and alternating temperatures.
In such studies, the alternation of temperature can produce
three types of responses: (1) lower percentage of
germination (Rojas-Aréchiga et al. 1997, 1998, 2001,
Matías-Palafox 2007, Ortega-Baes & Rojas-Aréchiga 2007,
Lindow-López et al. 2018b), (2) similar percentage of
germination (Godínez-Álvarez & Valiente-Banuet 1998,
Ruedas et al. 2000, De la Barrera & Nobel 2003, Yang et al.
2003, Ramírez-Padilla & Valverde 2005, Matías-Palafox
2007, Sánchez-Soto et al. 2010, Ortega-Baes et al. 2011,
Mazzola et al. 2013, Jiménez-Sierra & Matías-Palafox
2015, Kin et al. 2015, Lindow-López et al. 2018b) or (3)
higher percentage of germination (Godínez-Álvarez &
Valiente-Banuet 1998).
In some studies, the three types of responses have been
observed (Ortega-Baes et al. 2010, Meiado et al. 2016).
From these results, it can be inferred that the germination
response concerning the constancy or variation of the
temperature becomes species-specific (Ortega-Baes et al.
2010) so that a general tendency does not exist in the
Cactaceae family such as in other families (Baskin &
Baskin 2014).
Some studies of the 1990s (Cancino et al. 1993, Nolasco
et al. 1996, Vega-Villasante et al. 1996) demonstrated that
exposing Pachycereus pringlei and P. pecten-aboriginum
seeds to temperatures from 55 to 70 °C for various hours,
days or even weeks prior to sowing; left some seeds viable.
Studies performed on 17 species (Table 1), with seeds that
have been exposed to temperatures between 60 - 90 °C
(Ruedas et al. 2000, Olvera-Carrillo et al. 2003, Mandujano
et al. 2005, Ramírez-Padilla & Valverde 2005, Sánchez-
Soto et al. 2010, Pérez-Sánchez et al. 2011), found four
types of response: a) For Isolatocereus dumortieri at 70 °C
the final germination percentage decreased (Pérez-Sánchez
et al. 2011); b) For Mammillaria magnimama, decreasing
only occurred in lots of old seeds (Ruedas et al. 2000);
c) For several species, the most common response was to
show similar germination than in the controls (Ruedas et al.
2000, Olvera-Carrillo et al. 2003, Ramírez-Padilla &
Valverde 2005, Sánchez-Soto et al. 2010); d) For several
species the exposure to high temperatures exceeded the final
germination of the control (Olvera-Carrillo et al. 2003,
Sánchez-Soto et al. 2010, Pérez-Sánchez et al. 2011),
demonstrating cactus seed tolerance to high temperatures, at
least for short periods. The seed tolerance to extreme
temperatures may have evolved as a mechanism to enable
persistence in the soil in predominantly desert species with
high temperatures on the soil surface (Daws et al. 2007).
In recent years, various studies of cactus have directed
their efforts to evaluating the possible impact of global
warming on the germination of the seeds (Ordoñez-
Salanueva et al. 2015, Flores et al. 2017, Gurvich et al.
2017, Seal et al. 2017, and Aragón-Gastélum et al. 2018),
through the assessment of the germination response faced
with different temperatures. Other studies, although not
directly mentioning global warming, show useful results to
evaluate the response of cactus seeds faced with
temperatures higher than 30 °C (Kin et al. 2015, Meiado et
al. 2016). However, conclusions are ambiguous.
The results shown by Seal et al. (2017) showed a possible
explanation for the ambiguity of the response of cacti seeds
to high temperatures. That study showed the tendency of
species that inhabit temperate environments (extratropical
or tropical cactus species that inhabit altitudes > 1,000 m
asl) possess optimal germination temperatures generally,
between 5 and 10 °C of difference above the average of the
period when germination occurs. This study revealed the
capability of thermal buffering for the germination that
these species possess. Although Seal et al. (2017) only
included a few species that inhabit warm environment
(tropical species that grow between 0 - 1,000 m asl.) the
aforementioned species were shown to possess near optimal
germination temperatures, generally between 1 and 3 °C of
difference or slightly lower than the current average in the
rainy period (Seal et al. 2017). For these species, the models
predict an impact through the increase of the temperatures
for the RCP 8.5 scenario (of greater warming) and in some
cases until the RCP 2.6 scenario (of lower warming) (Seal
et al. 2017).
Most germination studies performed on cacti, where
different temperatures are compared, generally include
species that inhabit temperate environments (Seal et al.
2009, 2017). Seal et al. (2009) gathered information about
germination from approximately a hundred cacti with
values between 30 and 41 °C, but only 12.6 % were species
from warm climates. From this compilation, it can be
deduced that both the cactus species that inhabit temperate
climates and those of warm climates generally possess a
similar response to this temperature range.
The germination study that included the greatest quantity
of tropical cacti species was performed by Meiado et al.
(2016) with 30 species, mostly endemic of the Caatinga in
Brazil. These authors found a germination response higher
than 50 % to temperatures of 35 °C and an optimal
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425
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temperature around 30 °C, which is a temperature near or
slightly higher than the average temperatures reported for
that region according to Da Silva (2004). Although it could
be expected that the cactus species that inhabit temperate
environments have a lower optimal germination temperature
than species that inhabit warmer environments, the
information available shows that both cacti groups generally
possess a similar germination response to 30 °C (Figure 4).
Figure 4. Seed germination responses at 30 °C between cacti from
temperate and warm climates, based on 43 data from temperate and
34 from warm climate.
This similar response implies that the cactus species of
temperate climates possess the greatest capacity for thermal
buffering of germination, as the results of Seal et al. (2017)
suggest. The warm climate species, being within the limit or
very close to the optimal germination temperature will
possess a lower capacity for buffering and in consequence it
will possibly be these cacti that are the most vulnerable to
the effects of the expected climatic change.
Light and seed germination. The germination response
considering conditions of light and darkness has been
assessed in 275 cactus species (Table 1). So far no negative
photoblastic seeds have been found in cacti and 80.9 %
have presented positively photoblastic seeds (Matías-
Palafox & Jiménez-Sierra 2006, Flores et al. 2006, 2011,
Cheib & Souza 2012, Delgado-Sánchez et al. 2013, Rojas-
Aréchiga et al. 2013, Meiado et al. 2016). Among the cacti
with indifferent or neutral photoblastic seeds, 34 taxa have
been reported in the Cactoideae subfamily that represent
only 13.8 % of its species, however, 75 % of the 24 taxa
studied of the subfamilies Opuntioideae, Pereskioideae and
Maihuenioideae, have indifferent photoblastic seeds, which
suggests that this character is ancestral in Cactaceae.
Several studies indicate a strong influence from
phylogeny in the photoblastic response within the family
(Flores et al. 2011, Rojas-Aréchiga et al. 2013, Meiado et
al. 2016). Rojas-Aréchiga et al. (2013) found a
phylogenetic influence between various species of the
Cacteae tribe, while Flores et al. (2011) found that the
Cacteae, Pachycereeae and Trichocereeae tribes include
species with greater germination response to light than in
Notocacteeae. On the other hand, Meiado et al. (2016)
found that the phylogenetic origin was the only variable
influencing the germination response to light in 30 cactus
species of Brazil, and only the species of Pereskioideae and
Opuntioideae showed an indifferent photoblastic response,
while all the Cactoideae species were positively
photoblastic.
The seed response to light in Cactaceae has traditionally
been evaluated in association with the form of life (Rojas-
Aréchiga et al. 1997, Ortega-Baes et al. 2010, Flores et al.
2011), size and seed mass (Flores et al. 2006, Ortega-Baes
et al. 2010, Rojas-Aréchiga et al. 2013), as well as to
different wavelengths or solar irradiation (Alcorn & Kurtz
1959, McDonough 1964, Zimmer 1969a, 1973, Rojas-
Aréchiga et al. 1997, Nolasco et al. 1997, Benítez-
Rodríguez et al. 2004, Olvera-Carrillo et al. 2009, Meiado
et al. 2010, Zerpa-Catanho et al. 2019) and concentrations
of gibberellins (Alcorn & Kurtz 1959, McDonough 1964,
Rojas-Aréchiga et al. 2001, Ortega-Baes & Rojas-Aréchiga
2007, Rojas-Aréchiga et al. 2011, Mascot-Gómez et al.
2020). Some preliminary studies suggested that an
association between the life-form and the photoblasticism
could exist (Rojas-Aréchiga et al. 1997, Rojas-Aréchiga &
Vázquez-Yanes 2000). Other research has subsequently
opposed that hypothesis (Ortega-Baes et al. 2010, Flores et
al. 2011, Meiado et al. 2016). Moreover, Flores et al. (2011)
found a negative relationship between the germination
response to light and the height of the plant, probably
because tall cacti produce larger seedlings than short cacti
(Flores et al. 2011). Similar readings can be obtained from
the data of Rojas-Aréchiga et al. (1997).
Several cactus studies have shown a relationship between
seed size and the requirement of light to germinate (Maiti et
al. 2003, Sánchez et al. 2015). Both Flores et al. (2006) and
Ortega-Baes et al. (2010) considered that positive
photoblastism in the 37 cactus species they studied could be
related to the small size of their seeds and their potential for
building soil seed banks. Similarly, Flores et al. (2011)
obtained a negative relationship between seed mass and the
dependence on light to germinate; nevertheless, in species
without dormancy this relationship was marginal or non-
significant, which the authors attributed to the differences
that were presented between dormant and non-dormant
seeds or to the size of the sample.
Some previous studies of around 80 species of cacti
(Rojas-Aréchiga et al. 2013, Meiado et al. 2016) found no
relationship between the requirement of light for
Seed traits and germination in the Cactaceae
426
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germinating and seed size. Probably these results with a
certain ambiguity could be explained by the small size and
mass that cacti show in general and because the role of the
phylogenetic relationships (as already referred to) can
distort the interpretation of the data.
The influence of gibberellic acid (AG3) as a light
substitute has been studied in cacti since Alcorn & Kurtz
(1959) found that a fraction of positively photoblastic seeds
of Carnegiea gigantea were stimulated in darkness with the
addition of AG3. Subsequently, McDonough (1964)
confirmed the aforementioned results and also included
Stenocereus thurberi with similar results. Similar findings
have been found in several cactus genera by Brencher et al.
(1978), Arias & Williams (1978), Zimmer & Büttner (1982)
and López-Gómez & Sánchez-Romero (1989).
Nevertheless, even though the role of AG3 has not been
subsequently studied (Ortega-Baes & Rojas-Aréchiga 2007,
Rojas-Aréchiga et al. 2011), the works that refer to it in
cacti have not found a stimulation of germination under
darkness (Williams & Arias 1978, Arias & Lemus 1984,
Rojas-Aréchiga et al. 2001, 2011, Olvera-Carrillo et al.
2003, Ortega-Baes & Rojas-Aréchiga 2007, Rojas-Aréchiga
2008, Mascot-Gómez et al. 2020). Even when the AG3
effect as a promoter of germination under white light has
been evaluated, in the majority of the studies an enhancer
effect on different concentrations in intact seeds has not
been found (Mandujano et al. 2007, Ortega-Baes & Rojas-
Aréchiga 2007, Rojas-Aréchiga 2008, Olvera-Carrillo et al.
2009, Amador-Alférez et al. 2013, Loustalot et al. 2014,
Rodríguez-Ruíz et al. 2018, Gonzalez-Cortés et al. 2018).
The difficulty in clearly establishing the role of AG3 as a
germination promoter for Cactaceae could be related to the
fact that in the studies homogeneity has not been maintained
in the following parameters: light conditions, age of the
seeds, types of dormancy, time and mode of application of
the AG3 concentrations, among others. These differences
among parameters can include changes in the behavior of
seeds' germination in the species and thus hinder the
comparisons among the performed studies (Rojas-Aréchiga
2008). Nevertheless, possibly AG3 does not possess such an
important role as a germination promoter in cacti seeds,
such as Rojas-Aréchiga (2008) and Rojas-Aréchiga et al.
(2011) refer to.
Water and saline stress and germination. In general, seeds
of most plants studied stop germinating at water potentials
between -0.5 and -2.0 MPa (Dürr et al. 2015, Tribouillois et
al. 2016). These potentials are experimentally achieved with
the use of different concentrations of three main substances:
mannitol (Maldonado et al. 2002, Guerrero et al. 2016),
polyethylene glycol (PEG) (Yang et al. 2010, Luna &
Chamorro 2016, Pantané et al. 2016) and NaCl (Zhang et
al. 2010, Gorai et al. 2014, El-Keblawy et al. 2016).
In cacti, only four studies have assessed the germination
at water potentials lower than -1.0 MPa (Martins et al.
2012, Guerrero et al. 2016, Aragón & Lasso 2018, Zerpa-
Catanho et al. 2019), maybe because in most cases the
species do not achieve germination at such potentials
(Flores & Briones 2001, Ramírez-Padilla & Valverde 2005,
De La Rosa-Manzano & Briones 2010, Guillén et al. 2011,
2015, Rodríguez-Morales et al. 2013, Flores et al. 2017,
Bispo et al. 2018). The studies in cacti reveal that
germination mainly occurs at water potentials between
0 and -0.6 MPa (Figure 5) and at temperatures of 25 to
30 °C (Vega-Villasante et al. 1996, Kin et al. 2015, Gurvich
et al. 2017, Flores et al. 2017, Bispo et al. 2018).
Figure 5. Seed germination response under water stress. Data are
based on 28 cactus species studied.
In some species, it has been observed that the water
potentials of -0.2 MPa (Guillén et al. 2009, 2015, Gurvich
et al. 2017, Flores et al. 2017) or even -0.4 MPa (Flores &
Briones 2001, Guillén et al. 2011, 2015, Flores et al. 2017)
or -0.6 MPa (Flores & Briones 2001) favor germination.
Nevertheless, generally water potentials lower than
-0.6 MPa notably decrease the percentage of germination
(Meiado et al. 2010, Guillén et al. 2011, 2015, Gurvich et
al. 2017, Flores et al. 2017, Bispo et al. 2018). Thus, cactus
seeds adapted to germinate at high soil moisture, but not
necessarily at the soil field water capacity, would have an
advantage germinating in arid environments. However, this
may have a trade-off between germination at relatively low
soil water potential and seedling establishment because
seedlings generally require higher soil water potential to
compensate for transpiration (Flores & Briones 2001).
In addition, in the species where the effect of water
potential and temperature has been combined, normally at
25 °C, better results have been obtained than at
temperatures of 30 °C or higher (Oliveira et al. 2017,
Gurvich et al. 2017, Flores et al. 2017, Bauk et al. 2017).
For primarily arid and semiarid species with small seeds, as
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occurs in Cactaceae, the preference for germinating in
humid soil can be an advantage that permits to reduce
seedling mortality when faced with transient rain followed
by prolonged droughts. These conditions could favor
germination but could also result in death of seedlings
through subsequent drought (Venable & Lawlor 1980).
Approximately a dozen studies (Table 1) have evaluated
the germination response of cacti faced with conditions of
salinity (Romero-Schmidt et al. 1992, Vega-Villasante et al.
1996, Nolasco et al. 1996, Meiado et al. 2010, Martins et al.
2012, Ortiz et al. 2014, Lima & Meiado 2017, Podda et al.
2017, Bispo et al. 2018). A germination response in the
range of 0 to -0.6 MPa with NaCl is similar to the results
obtained with PEG, even though there are species where the
germination percentages with NaCl are higher than in a
similar osmotic potential of PEG (Meiado et al. 2010, Bispo
et al. 2018). In other cases, the seeds germinate better in
PEG (Martins et al. 2012). On the other hand, there is very
little information about the application of the hydrotime
model to evaluate the effects of water or saline stress on
germination speed (or germination time) in cactus species
(see: Simão et al. 2010). Germination time is an important
feature of plant life history that determines germination
capacity under dry conditions and recruitment time
(Sánchez-Soto et al. 2005, Donohue et al. 2010, Dürr et al.
2015).
Hydration-dehydration cycles and germination. Two
pioneering studies of Dubrovsky (1996, 1998) demonstrated
the utility of the hydration-dehydration cycles in increasing
the speed and final percentage of germination in four cactus
species. However, still there are a few cactus studies (Table
1) that address these treatments as germination promoters
(Sánchez-Soto et al. 2005, Rito et al. 2009, Santini &
Martorell 2013, López-Urrutia et al. 2014, Contreras-
Quiroz et al. 2016a, 2016b, Santini et al. 2017, Lima &
Meiado 2017, 2018, Sánchez et al. 2018), although
hydration-dehydration cycles have been and are widely used
in innumerable species worldwide (Sánchez & Pernús
2018). The evaluation of this type of pre-germinative
treatment in cactus seeds should be tested more in the
future, because the seeds are subject to hydration-
dehydration cycles in nature, which can influence not only
germination but also aspects related to conditional or
cyclical dormancy, seed longevity and seedling survival,
among others (Baskin & Baskin 2014). Similarly, water
treatments (or cycles) could be implemented as
ecotechnologies in ecological restoration projects and in
conservation programs of germplasm (Sánchez & Pernús
2018).
The ability of seeds to maintain physiological changes
produced during hydration, such as differential protein
expression, through discontinuous dehydration periods
(López-Urrutia et al. 2014), has been called “hydration
memory” (Dubrovsky 1996). Contreras-Quiroz et al.
(2016b) evaluated this phenomenon in cacti from a semi-
desert area in northeastern Mexico, and from a sub-humid
area of central Argentina, and suggested that the presence of
hydration memory in the seeds of Cactaceae depends on the
climate and the microenvironment where the cacti occur,
indicating that environmental conditions imposed on the
parental plants influence the germination responses of the
cacti seeds when subjected to discontinuous hydration. This
hypothesis was corroborated by Lima & Meiado (2017)
who found that the seeds of the same species (Pilosocereus
catingicola subsp. salvadorensis) collected from
populations located in different ecosystems have different
germination responses after passage through discontinuous
hydration and HD cycles. This finding gives evidence that
“hydration memory” provides greater tolerance to
environmental stresses but with different responses among
populations.
Cactus seed dispersal. Rojas-Aréchiga & Vázquez-Yanes
(2000) reported six studies about cactus seed dispersion
through endozoochory. In the last two decades, a few more
than a dozen species have been studied regarding this type
of interaction and its effect on germination (Godínez-
Álvarez & Valiente-Banuet 2000, Montiel & Montaña 2000,
Godínez-Álvarez et al. 2002, Naranjo et al. 2003, Baraza &
Valiente-Banuet 2008, Pérez-Villafaña & Valiente-Banuet
2009, Casado & Soriano 2010, Fonseca et al. 2012, Gomes
et al. 2014, Nascimento et al. 2015, Lasso & Barrientos
2015, Vázquez‐Castillo et al. 2018, Santos et al. 2019).
Other types of cactus seed dispersal referred to by Rojas-
Aréchiga & Vázquez-Yanes (2000) as synzoochory
(Munguía-Rosas et al. 2009, Fonseca et al. 2012),
epizoochory (Lasso & Barrientos 2015) and hydrochory
(Lenzi et al. 2012, Sánchez-Salas et al. 2012, Sánchez-Salas
et al. 2013, Romero-Méndez et al. 2018) have been
reported in a small number of studies.
In vitro propagation. Although in a great number of cactus
species high percentages of germination have been found
(Zimmer 1969b, 1998, Meiado et al. 2016), various studies
have explored in vitro germination as an alternative of
propagation (Salas-Cruz et al. 2011, Xavier & Jasmim
2015, López-Escamilla et al. 2016, Cortés-Olmos et al.
2018, Ramírez-González et al. 2019). Studies of this type
have been performed on more than 40 cactus species (Table
1), with good results in germination and later seedling
growth. The in vitro germination with enriched resources
could be a necessary and essential method in the
propagation of rare species with few seeds or with a low
percentage of germination, both for preservation of the
species or another purpose.
Seed traits and germination in the Cactaceae
428
On line first
Seed storage at low temperatures. Although in the present
review the seed desiccation tolerance and the longevity of
cactus seeds have been commented on, few studies have
evaluated the seed preservation in controlled conditions.
Only in 20 species has a preservation at - 0 °C been
evaluated, up to a maximum of 13 months (Nolasco et al.
1996, Vega-Villasante et al. 1996, Veiga-Barbosa et al.
2010, Goodman et al. 2012, Marchi et al. 2013, Salazar et
al. 2013, Bárbara et al. 2015, Civatti et al. 2015, Dos Santos
et al. 2018). Studies of this type are necessary when faced
with the increasing threats that confront the family
(Goettsch et al. 2015) and the need to search for secure
alternatives for long-term preservation.
Concluding remarks. In the last two decades, the number of
studies related to cactus germination has increased
exponentially, with Mexico, Brazil and Argentina being the
three countries leading this scientific field. Seed
germination has been evaluated in less than 50 % of the
genera. Only physiological dormancy has been found in the
family. Terrestrial and aerial cactus seed banks have been
little studied but are perhaps common and play an important
role in the population dynamics of the species. The two
most studied research topics on cactus seed germination are
photoblasticism and the response to temperature. No cactus
with a negatively photoblastic response has been found, and
most of the species of the subfamily Cactoideae have
positively photoblastic seeds. The optimal temperature
range for cacti is found between 20 and 30 °C. However,
there are still genera with more than 20 species that have
not been studied such as Matucana, and others genera like
Frailea, Rebutia, and Selenicereus where only one species
has been studied.
There is not enough evidence on seed traits and cactus
seed germination, but seed shape has been related with seed
dispersal in that the hat-shaped seeds have been associated
with hydrochory. The relationships between cactus seed
germination and phylogeny depends on the species studied
and the tribe. The germination types or variants do not
appear to be related with seed germination percentage.
Cactus seeds are adapted to germinate at high soil moisture,
but not necessarily at the soil field water capacity. Seeds
germinate at saline potentials between 0 and -0.6 MPa.
Hydration-dehydration cycles or hydration memory increase
the speed and the final percentage of germination in some
species; the presence of hydration memory in the seeds of
Cactaceae depends on the climate and the
microenvironment where the cacti occur.
Preserving cactus seeds in banks is an encouraging
concept because their longevity in general surpasses six
months, and a high percentage of species possess seeds that
maintain their viability for periods between one to two years
without extreme storage requirements. Similarly, studies
about desiccation tolerance and cryopreservation that have
been performed demonstrate their feasibility. In the future, it
would be useful if more cactus germination studies included
measurement of seed traits, such as length, width and
compression, total dry mass, mass of the covering of the
embryo, moisture content, as well as imbibition rate.
Acknowledgements
The present study relied on support from the National
Botanical Garden, the Cuban Botanical Society and Planta!
The first author is grateful for the support received from R.
Rankin, L. R. González-Torres, A. C. González, J.L.
Aragón-Gastelum, M. V. Meiado and D. Franco for the
literature they sent. We appreciate the help of A. Ruiz
Fleitas with the seed drawings. We also thank the journal
editors and two anonymous reviewers whose work
contributed to improving the paper.
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________________________________________________
Associate editor: Arturo de Nova Vázquez
Authors' contributions: DB designed the review, compiled and
analyzed literature, made the figures, tables and wrote the first
version of the manuscript. JAS, JF and EJ also compiled the
literature and contributed to design the manuscript. All authors
made multiple revisions and approved the final versions of the
manuscript.
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