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Revista de Biología Tropical, ISSN: 2215-2075, Vol. 69(3): 843-851, July-September 2021 (Published Aug. 13, 2021)

Seed mass maturity in the terrestrial bromeliad Hechtia perotensis

(Bromeliaceae), endemic to Mexico

Violeta Elizalde

; https://orcid.org/0000-0002-4801-8782

José Rodolfo García

*; https://orcid.org/0000-0002-2086-1073

Carlos Trejo

; https://orcid.org/0000-0003-3431-4828

Cecilia Beatriz Peña-Valdivia

; https://orcid.org/0000-0003-4245-0547

Ma. Carmen Ybarra

; https://orcid.org/0000-0002-9634-008X

Otto Raúl Leyva

; https://orcid.org/0000-0002-6150-9367

1. Postgrado en Botánica, Colegio de Postgraduados, Campus Montecillo, Carretera México-Texcoco, km 35.5, Estado

de México, 56230, México; violetaelizalde@gmail.com, garcianr@colpos.mx (*Correspondence), catre@colpos.mx,

cecilia@colpos.mx

2. Departamento de Ingeniería Agroindustrial, Universidad Autónoma Chapingo, Carretera México-Texcoco km 38.5,

Estado de México, 56230, México; ycydrive@gmail.com

3. Facultad de Ciencias Biológicas y Agropecuarias, Universidad Veracruzana, Camino a Peñuela s/n. C.P.94945

Peñuela, Amatlán de los Reyes, Ver., México; oleyva@uv.mx

Received 13-VIII-2020. Corrected 29-IV-2021. Accepted 03-VIII-2021.

ABSTRACT

Introduction: H. perotensis is a plant with a high potential for ecological restoration because it yields thousands

of seeds and grows under low levels of rain, poor soils and contrasting temperatures. However, little is known

of the seed mass maturity (high seed germination, low seed fresh weight and low seed moisture content) in this

species.

Objective: Assess seed germination in the laboratory of H. perotensis during seed development and along the

floral stalk (infructescence) in two sites one in rocky location and another near a lake. The hypothesis was that

there is a time after flowering in which seeds have highest germination and fresh weight and that the apical,

centre and base of the infructescence are different in seed germination and fresh weight in both sites.

Methods: Capsules were collected in two sites one in rocky land (Frijol Colorado, Perote, Veracruz) and another

near one lake (Alchichica, Puebla), in the months of August, September and November 2016 and January 2017.

A repeated measure design (RMD) was used to analyze the effects of infructescence section on seed weight,

moisture content and seed germination (41, 87, 152 and 215 days after flowering). Each evaluation time com-

prised five replicates, each one with 15 seeds.

Results: Difference in seed germination, seed weight and moisture content between sections of the infructes-

cence was not significant. However, significant differences were found not only between first and last sample

dates, but mainly between first and second dates. Eighty-seven days after flower pollination seed moisture

content was lower than 20 % and up to 80 % of seed germinated in both sites of sampling.

Conclusions: In this study it was found that the moisture content of H. perotensis seed can be used as an indica-

tor of the physiological maturity of the seed and it is also related to germination of the seed.

Key words: ecological restoration; infructescence; moisture content; germination; seed weight.

Elizalde, V., García, J.R., Trejo, C., Peña-Valdivia, C.B., Ma.

Ybarra, C., & Leyva, O.R. (2021). Seed mass maturity in

the terrestrial bromeliad Hechtia perotensis (Bromeliaceae),

endemic to Mexico. Revista de Biología Tropical, 69(3),

843-851. https://doi.org/10.15517/rbt.v69i3.43477

https://doi.org/10.15517/rbt.v69i3.43477

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Revista de Biología Tropical, ISSN: 2215-2075 Vol. 69(3): 843-851, July-September 2021 (Published Aug. 13, 2021)

The genus Hechtia Klotzsch is one of

the more interesting members of the Mexican

Bromeliaceae because it is the only member

of the subfamily Hechtioideae and has experi-

ence recent discovery of new species (Ramírez

et al., 2014). The estimated number of species

in Mexico is 65 (Ramírez & Jiménez, 2012)

and 94 % of them are endemic (Ramírez et

al., 2014). Hechtia plants are terrestrial or

lithophile and can grow in volcanic rocks and

limestone hills. Bromeliaceae seeds are brown,

fusiform, rough, oblong, ellipsoids, one mm

wide and three mm long (Espejo et al., 2007).

Reyes (2015) suggests that Hechtia can be used

in ecological restoration programs because it

produces a remarkably high quantity of seeds

and the ability of plants to grow under low

rainfall, on poor soils, and under contrast-

ing temperatures. However, the knowledge of

Hechtia seed biology is limited (Espejo et al.,

2007). Information of seed moisture content,

dry weight, and seed germination after seed

mass maturity of H. perotensis has not been

reported. Information about the genus Hechtia

includes seed morphological descriptions of

H. nuusaviorum (Espejo et al., 2007) and new

species descriptions of H. schottii (Escobedo,

2012), H. santanae (Ramírez et al., 2016),

H. flexilifolia, H. huamelulaensis, H. nivea

(Ramírez et al., 2014).

Seed germination characteristics are fun-

damental for species conservation (Baskin &

Baskin, 1998). In consequence, it is necessary

to know the timing of seed harvest as it influ-

ences seed quality (physical and physiological)

and storage effects (Willan, 1985) to initiate

nursery programs and store seeds in germ-

plasm banks. Seed germination is sensitive to

environmental conditions (Leck et al., 2008).

Sankhla and Chawan (1980) found that seed

moisture content is important in regulating seed

germination. For example, Phaseolus trilobus

seeds had 100 % seed germination at 30 %

moisture content and 0 % with moisture con-

tent of 2 %. In addition, seed quality continues

to improve during development and even after

maximum dry weight (Pieta & Ellis, 1991) as

seen with seeds of beans (Sanhewe & Ellis,

1996) and cereals (Hay & Probert, 1995). Seed

development of H. perotensis has not been

reported and this, together with timing of seed

harvest is a first requirement to start propaga-

tion in nurseries and to store seeds with maxi-

mum seed quality in seed banks. The objective

of this research was to assess seed moisture

content, seed weight and seed germination of

H. perotensis during seed development in two

sites one in a rocky location and another near

a lake. The hypothesis was that after flower-

ing there is a time nearly at the end of seed

mass maturity where seeds have low weight

due to seed drying, low moisture content and

maximum germination. Also, that seed quality

differs among three longitudinal sections of the

infructescence due to differences in maturity

along the stalk.

MATERIAL AND METHODS

Sample sites: H. perotensis seeds were

collected at site 1 a rocky land, Frijol Colorado,

Perote, Veracruz (2 416 m.a.s.l, 19°32´13.95”

N & 97°22´98” W) and site 2, Tepeyahualco

at the lake of Alchichica, Puebla, México (2

326 m.a.s.l, 19°25’11” N & 97°23’56” W)

(geolocation with Garmin eTrex 10 & Google

Earth

) (Google Earth, n.d.-a; Google Earth,

n.d.-b). The sites were selected to investigate

the effect of the lake (site 2) in the relative

humidity and on seed mass maturity compared

with site 1 plants growing in rocky land. The

climate of each region is semiarid with warm

summers BS1kw(i´)gw” (García, 1988). The

vegetation is typical of a xeric shrublands

(Ramírez et al., 2014). Soil was alkaline, not

saline, loamy and poor in nutrients in both sites

(laboratory analysis).

Plant selection: In a first visit in June

2016 thereafter called day 0, male and female

plants in both sites had flowers and insect

pollinations. After one month, plants of both

sites had green immature capsules and at this

moment a white perforated sleeve shape cloth

with diameter of 1 mm was inserted along

the infructescence in order to keep the seeds

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inside the cloth in case of dehiscence. Each

infructescence length was registered with a

measuring tape, divided in three and adjust-

ing a lace in each section to keep the mature

seeds separated.

Capsule sampling: Capsules of H. pero-

tensis in both sites were collected in August,

September, November 2016 and January 2017.

The mean temperature was 15.3 and 17.6 °C,

and mean relative humidity for 56.8 and 60 %

(data logger Hobo), of site 1 and 2, respectively

during the sample months. Temperature and

relative humidity were measured to compare

the environment characteristics.

Once capsule colour changed from green

to brown around 41 d after flowering (DAF) 25

capsules were harvested from each of the base,

centre, and apex of the infructescence. Two to

four capsule sample dates were made according

to the availability of capsules. Samples were

made at 41, 87, 152 and 215 DAF in plants

named A in site 1 and B in site 2. Plant named

C and D of site 1 and 2 respectively were

sampled at 41 and 87 DAF due to less avail-

ability of capsules.

Seeds extracted from capsules with fine

clippers were stored at (25 ± 1 °C) in seal

aluminium bags. Seed weight, humidity and

germination evaluations were made within one

week after each harvest period.

Seed weight: Seed weight was determined

in 225 seeds by infructescence in a precision

balance (± 0.0001 g; Scientech SA 120) taking

75 seeds from the apex, centre and base of the

infructescence this procedure was repeated for

each sample date.

Seed moisture content: Seed fresh weight

of five replicates each with 15 seeds was deter-

mined from the apex, centre, and base of the

infructescence this procedure was repeated for

each sample date. Seeds were kept at 50 ± 1 °C

in an oven until they reach constant weight (5

d). Seed moisture content was calculated using

the following expression (International Seed

Testing Association, 2010).

Seed moisture content = Seed fresh weight – Seed dry weight x 100

Seed fresh weight

Germination: Seeds were placed in petri

dishes with filter paper on the bottom and 10

mL of distilled water was added. Five repli-

cates with fifteen seeds (per petri dish of 14 cm)

were tested from the apex, centre, and base of

the infructescence this procedure was repeated

for each sample date. Seeds were superficially

disinfested by immersion in sodium hypochlo-

rite (60 g/L of Cl active for 1 min) 1 % (v:v in

water). Petri dishes were placed in an incuba-

tor (Thermo Scientific. USA: model 846) set

at 25 ± 1 °C and photoperiod of 12 h darkness

x 12 h light (12 μmol m

-2

-1

of irradiation). A

seed was considered germinated when 1 mm

of radicle was exposed using a digital caliper

Vernier. Evaluations were made at 8 and 15 d

from placement in the incubator (International

Seed Testing Association, 2010).

Seeds in development: Seeds were

observed with a stereo microscope (Leica EZ4

HD) to identify embryo development this pro-

cedure was repeated for each sample date. Seed

testa was dissected near the embryo and the

embryo was extracted with tweezers (Interna-

tional Seed Testing Association, 2010).

Experimental design: A repeated mea-

sures design (RMD) was used to analyze the

effects of time (day 41, 87, 152 and 215)

and infructescence section on seed weight,

moisture content, seed germination and seed

development at each site. Each evaluation time

comprised five replicates each of 15 seeds

as an experimental unit from the apex, cen-

tre, and base of the infructescence. Multiple

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Fig. 1. A. B. C. and D. Germination, seed moisture content, seed fresh weight and seeds in development from the plant A

site 1 (Frijol Colorado, Perote, Veracruz) and E. F. G. and H of plant B, from site 2 (Tepeyahualco at the lake of Alchichica,

Puebla). Each column represents the average of 5 replicates of 15 seeds each. The apex ( ), centre ( ) and base ( ) of the

stalk is represented by three columns. The letters on the columns represent the effects of the time in each section of the stalk

by date of days after flowering.

comparisons were made with the general lineal

model (α = 0.05).

RESULTS

Plant A site 1 Frijol Colorado, Perote,

Veracruz: Seeds of the three sections of the

stalk (base, medium and apex) were similar on

germination, moisture content and seed fresh

weight (Fig. 1A, Fig. 1B, Fig. 1C) in each date

sampled (P > 0.05). However, there was statisti-

cal difference over time; at 41 DAF seed fresh

weight average at three sections was 0.0360 g,

moisture content of 76 % and seed germina-

tion of 20 %. Whereas seeds sampled at 215

DAF had seed fresh weight average at the three

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sections of 0.0139 g, seed moisture content of

6 % and 94 % of seed germination (P ≤ 0.05).

Seeds in development were similar in the three

sections of the stalk at 41 DAF with an average

of 80 % of seeds. At 87, 152 and 215 DAF seeds

in development were on average 6 % without

differences in the sections of the stalk (Fig. 1D).

Plant B site 2 Tepeyahualco at the lake

of Alchichica, Puebla: Seed germination,

moisture content and seed fresh weight (Fig.

1E, Fig. 1F, Fig. 1G) was similar in the three

sections of the stalk in each date sampled, how-

ever seed germination, moisture content and

seed fresh weight showed evident differences

with time. On average, seed germination at 215

DAF (98 %) was 2.6 times higher than that at

41 DAF (37 %) (Fig. 1E). Conversely, seed

moisture content diminished from 69 to 6 %,

nearly ten times in the same period (Fig. 1F).

Seed fresh weight (Fig. 1G) was different

(P ≤ 0.05) in the three sections of the stalk over

time. The average seed fresh weight was more

than double at 41 DAF (0.036 g) compared

with 215 DAF (0.016 g) this decrease of seed

moisture was due to seed drying.

Seeds in development were similar in the

three sections of the stalk at 41 DAF with an

average of 60 % of seeds. At 87, 152 and 215

DAF seeds in development were on average

4 % without differences in the sections of the

stalk (Fig. 1H).

Plant C site 1 Frijol Colorado, Perote,

Veracruz: Seeds of the three sections of the

stalk did not differ in germination, moisture

content and seed fresh weigh at 41 and 87 DAF

(Fig. 2A, Fig. 2B, Fig. 2C) (P > 0.05). How-

ever, the average seed germination at 41 and 87

DAF was 23 and 95 % respectively (Fig. 2A).

Seed moisture content and seed fresh weight

of the three sections on average was 72 % and

0.035 g at 41 DAF. At 87 DAF seed moisture

content diminished to 29 % and seed fresh

weight was 0.017 g (Fig. 2B, Fig. 2C).

Seeds in development were similar in the

three sections of the stalk at 41 DAF with an

average of 76 % of seeds. At 87 DAF seeds

in development were on average 4 % without

differences between the sections of the stalk

(Fig. 2D).

Plant D site 2 Tepeyahualco at the lake

of Alchichica, Puebla: Seed germination,

moisture content and seed fresh weight (Fig.

2E, Fig. 2F, Fig. 2G) was similar in both dates

sampled. Also, seed moisture content and seed

fresh weight differed over time (P ≤ 0.05), but

not between stalk sections. The average seed

germination of the stalk was 83 % at 87 DAF

(Fig. 2E). Seed moisture content and fresh

weight (Fig. 2F, Fig. 2G) decreased to 9 %

and 0.0144 g respectively averaged across, the

three sections of the stalk at 87 DAF.

Seeds in development were similar in the

three sections of the stalk at 41 DAF with an

average of 35 % of seeds. At 87 DAF seeds

in development were on average 15 % differ-

ing between the apex and centre or base of the

stalk (Fig. 2H).

DISCUSSION

Our research showed homogeneity and

high seed germination (87 %) of H. perotensis

at 87 DAF at the two sites of seed collection

and across three sections of the infructescence.

In previous research Elizalde et al., (2017)

showed variation of seed germination of H.

perotensis from two different harvest dates (20

% in 2012 and 92 % in 2015), and as a conse-

quence, it was necessary to establish the time at

which H. perotensis reaches high seed quality.

Gutterman (1980) confirmed that seed

position in the fruit or infructescence is impor-

tant for seed germination. The perennial shrub

Mesembryanthemum nodiflorum had different

seed germination according to the position of

the infructescence in which the seed grows.

For example, in the apex seed germination was

of 61 %, in the centre 5.5 % and in the base 1

%. M. nodiflorum grows in the desert and the

difference in germination of the fruit is related

with the cycle life of this plant. As a conse-

quence, undetermined factors could have influ-

enced seed quality along an infructescence,

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such as environmental conditions during the

development of the mother plant, flower aper-

ture, and occurrence of pollination insects

(Gray & Thomas, 1982).

In contrast, Gesch et al., (2016) did not

find differences in seed germination between

different seed positions in plants of Thlaspi

arvense L. Similarly, in our research seeds of

H. perotensis did not show such locational dif-

ferences in germination.

Willson and Price (1977) found that pro-

duction of more flowers in one plant attracts

more pollinating insects and as a result plant

produce more seeds. McKinney et al., (2012)

showed that flowering timing coincides with

activity of pollinating insects to improve

Fig. 2. A. B. C. and D. Germination, seed moisture content, seed fresh weight and seeds in development from the plant C,

site 1 (Frijol Colorado, Perote, Veracruz) and E. F. G. and H of plant D from site 2 (Tepeyahualco at the lake of Alchichica,

Puebla). Each column represents the average of 5 replicates of 15 seeds each. The apex ( ), centre ( ) and base ( ) of the

stalk is represented by three columns. The letters on the columns represent the effects of the time in each section of the stalk

by date of days after flowering.

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homogenous flower pollination (Hegland et al.,

2009). H. perotensis was flowering with polli-

nation insects and we assumed that flower pol-

lination was efficient. In addition, the capsule

formation was homogenous in the three sec-

tions of the stalk mainly in seed germination.

Seed moisture content diminished gradu-

ally during seed development: the reserves are

accumulated (sugars) and solutes (proline) in

the vacuole and there is water displacement to

protect cell membranes. After, physiological

seed maturity (mass maturity) orthodox seeds

increase the process of seed drying to reach the

end of seed maturation (Bewley et al., 2013).

We found that seeds of H. perotensis improved

seed germination by about 80 % when seed

moisture content decrease to 20 % at the last

sample analyzed. H. perotensis seeds drying in

an environment with low relative humidity (60

%) and a medium temperature 16 °C, reaching

a low moisture content in about 45 days.

Bhawna et al., (2011) indicated that seed

maturity of Prunus cerasoides was at seed

moisture content of 31.96 % ± 1.42 %. Accord-

ing to Mai-Hong et al., (2003) 100 % seed ger-

mination of Peltophorum pterocarpum (DC) K.

Heyne is reach when seed moisture content was

56 % with maximum seed dry weight of 0.5 g.

The seed moisture content has been used as a

reliable indicator of seed maturity in several

studies e.g., by Shah et al., (2010). In our study

we found that seed moisture is an indicator of

seed maturity in H. perotensis. Harvest seeds

at 41 DAF were in development with an aver-

age moisture content of 70 %. Seeds reached

embryo maturity and increased germination at

87 DAF with only 10 % of seeds in develop-

ment. At this stage, maturation is approaching

and maturation drying is the event for orthodox

seeds to enter in a metabolic quiescent state.

Seeds can remain in this state for days to years

with high viability (Bewley et al., 2013).

Shah et al., (2006) showed that seed mois-

ture content of 23.4 to 36.1 % can be associated

with an optimum seed germination of Pyracan-

tha crenulata. Bewley et al., (2013) reported

that seed physiological maturity (vigour and

seed germination) is reached when seed dry

weight is greatest, and after this moment seeds

start to decrease in quality. For example, in

soya seeds maximum dry weight was obtained

45 d after flowering. For seeds of Caesalpinia

lutea and C. wrightii physiological maturity

was reached around 18 to 21 d after flowering

(Kaliangile & Grabe, 1988). Our results agree

with the above authors and demonstrated that

H. perotensis reach minimum seed fresh weight

(low seed moisture content) with coincidence

of maximum seed germination at the end of the

samples periods (87 DAF).

Maturity of seeds also has been associated

with seed moisture content, for example, Rici-

nus communis L. seed maturity was reported to

occur at 22 % seed moisture content (Vallejos

et al., 2011). Seeds of Aesculus indica Colebr,

Albizzia lebbeck and Celtis australis had physi-

ological maturity at 58, 52 and 32 % seed mois-

ture content respectively (Majeed et al., 2010;

Bhardwaj et al., 2002). Our research showed

that seeds of H. Perotensis reached physiologi-

cal maturity with fresh seed weight of 0.010

to 0.015 g, moisture content lower than 20 %

and seed germination of 85 %. Similar results

of seed fresh weight were reported by Elizalde

et al., (2017), however they mainly focused on

methods to improve seed germination.

Sankhla and Chawan (1980) claim that

seeds with high moisture content could produce

low seed germination. The authors explained

that a seed before drying is in development

with immature embryos and in the process of

storage of nutritive reserves. Therefore, seed

drying is necessary to reach high germination

percentages and seed maturity. After seed dry-

ing the events of seed development stop and

with seed water uptake the seed germination

metabolism starts (Bewley et al., 2013).

We conclude that H. perotensis reached

seed mass maturity 87 d after flowering with

20 % moisture content. With this knowledge

the point of harvest of seeds can be used to

store seeds with high percentage of germina-

tion in seed banks and to start a plant nursery

and use H. perotensis for ecological restora-

tion in their origin place and has the potential

to use this plant in other regions with similar

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environments. Both sites studied reached high

seed germination at the same time.

Ethical statement: authors declare that

they all agree with this publication and made

significant contributions; that there is no con-

flict of interest of any kind; and that we fol-

lowed all pertinent ethical and legal procedures

and requirements. All financial sources are

fully and clearly stated in the acknowledge-

ments section. A signed document has been

filed in the journal archives.

ACKNOWLEDGMENTS

To the Consejo Nacional de Ciencia y Tec-

nología (CONACYT) for the scholarship for

the first author. Many thanks to the reviewers

and editor that help to improve the manuscript.

RESUMEN

Madurez de las semillas en la bromelia terrestre

Hechtia perotensis (Bromeliaceae), endémica de México

Introducción: H. perotensis es una planta con un alto

potencial para la restauración ecológica debido a que pro-

duce miles de semillas y crece con niveles bajos de lluvia,

suelos pobres y temperaturas contrastantes. Sin embargo, el

desarrollo de la madurez de las semillas (germinación alta,

baja humedad y bajo peso fresco de semilla) en esta especie

es muy poco conocido.

Objetivo: Evaluar la germinación en el laboratorio de las

semillas de H. perotensis, durante el desarrollo de la semi-

lla y a lo largo del tallo floral (infrutescencia) en dos sitios;

uno en un área rocosa y otro cerca de un lago. La hipótesis

fue que hay un tiempo después de la floración, en el que

las semillas presentan la mayor germinación y menor peso

fresco, y que las secciones apical, central y base de la infru-

tescencia, la germinación y el peso fresco de la semilla son

diferentes en los dos sitios.

Métodos: se recolectaron las cápsulas en dos sitios uno

en un área rocosa (Frijol Colorado, Perote, Veracruz) y

otro cerca de un lago (Alchichica, Puebla), en los meses

de Agosto, Septiembre y Noviembre de 2016 y Enero de

2017. Se usó un diseño de medidas repetidas (DMR) para

analizar los efectos de la sección de la infrutescencia sobre

el peso fresco de la semilla, el contenido de humedad y la

germinación de la semilla (41, 87, 152 y 215 días, después

de la floración). Cada tiempo de evaluación comprendió

cinco réplicas y 15 semillas.

Resultados: La diferencia en la germinación de la semilla,

el peso de la semilla y el contenido de humedad entre las

secciones de la infrutescencia no fue significativa. Sin

embargo, se encontraron diferencias significativas entre

las fechas de muestreo inicial y final, pero sobre todo entre

la primera y la segunda fecha. Asimismo, ochenta y siete

días después de la polinización de las flores, el contenido

de humedad de las semillas fue inferior al 20 % y superior

al 80 % en la germinación de las semillas en ambos sitios

de muestreo.

Conclusiones: en este estudio se encontró que el contenido

de humedad de la semilla de H. perotensis, puede usarse

como un indicador de la madurez fisiológica de la semilla y

también está relacionado con la germinación de la semilla.

Palabras clave: restauración ecológica; infrutescencia;

contenido de humedad; germinación; peso de semilla.

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