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Annals of Applied Biology ISSN 0003-4746

RESEARCH ARTICLE

Phenological growth stages of edible asparagus (Asparagus


officinalis): codification and description according
to the BBCH scale
C. Feller1 , E. Richter2 , T. Smolders3 & A. Wichura4
1 Leibniz-Institute of Vegetable and Ornamental Crops, Department of Modelling and Knowledge Transfer, Großbeeren/Erfurt e.V., Großbeeren,
Germany
2 Julius Kühn-Institute, Federal Research Centre for Cultivated Plants, Institute for Plant Protection in Horticulture and Forests, Braunschweig, Germany
3 Limseeds BV, Horst, The Netherlands
4 Chamber of Agriculture Lower Saxony, Plant Protection Service, Hannover, Germany

Keywords Abstract
Asparagus; BBCH scale; phenological growth
stages. BBCH [Biologische Bundesanstalt (Julius Kühn-Institut), Bundessortenamt,
CHemische Industrie] scales are used in applied natural sciences for the
Correspondence description of phenological growth stages of plants and are available for
C. Feller, Leibniz-Institute of Vegetable and many crops today. Currently, a specific BBCH scale for Asparagus officinalis, a
Ornamental Crops, Department Modelling and
perennial vegetable plant of worldwide interest, does not exist. In this study,
Knowledge transfer, Großbeeren/Erfurt e.V.,
Theodor-Echtermeyer-Weg 1, 14979
an extended BBCH scale was developed, describing precisely the growth stages
Großbeeren, Germany. of A. officinalis. Nine principal growth stages were defined and subdivided into
Email: feller@igzev.de several secondary growth stages resulting in a two-digit decimal code. Detailed
descriptions of the particular stages and illustrations were included to clarify the
Received: 31 May 2011; revised version application of the code system. The scale is proposed to specify and harmonise
accepted: 29 November 2011. research activities as well as to enhance comparability of crop management
doi:10.1111/j.1744-7348.2012.00530.x practices for growers of asparagus.

Introduction
years, more and more plant species were added and
Knowledge of the phenology of cultivated plants is described according to the extended BBCH scale (Meier
not only important for agricultural and horticultural et al., 2009a; Archontoulis et al., 2010; Attibayéba
science but also for related scientific fields such as et al., 2010; Niemenak et al., 2010; Saska & Kuzovkina,
meteorological sciences and botany (Meier et al., 2009b). 2010). Although BBCH scales exist for many vegetable
The BBCH [Biologische Bundesanstalt (Julius Kühn- plants (Feller et al., 1995a,1995b), vegetable asparagus,
Institut), Bundessortenamt, CHemische Industrie] scale Asparagus officinalis L., has not been included until now.
is primarily based on a code originally developed for This article describes phenological growth stages of edible
cereal crops by Zadoks et al. (1974). The basic principles asparagus using the extended BBCH scale. The purpose
of the BBCH scale were described in detail by Hack et al. of the scale is to enhance comparability of research
(1992). In most cases, it consists of a decimal code, divided activities and to improve cultivation management for
into principal and secondary growth stages, although a scientists, advisers and growers around the world.
further division into mesostages is possible if necessary Some specific morphological features have to be
(Meier et al., 2009a). Meier (1997) and Meier et al. taken into consideration when working with asparagus.
(2009b) showed the substantial benefit of the BBCH scale A. officinalis belongs to the Asparagaceae family and is a
in agricultural practices and science, especially for the perennial dioecious plant with male and female flowers
correct timing of management events such as fertilisation on separate plants, although hermaphrodite flowers are
and pesticide applications to control pests, diseases and sometimes found (Lee et al., 1996; Ainsworth, 2000). The
weeds. subterranean part of the herbaceous plant is known as the
Meier et al. (2009b) gave a comprehensive overview crown, the foliage as the fern (Robb, 1984). Asparagus
of the general history of the BBCH codes. In recent foliage consists of many shoots or stems. The mature

174 Ann Appl Biol 160 (2012) 174–180 © 2012 The Authors
Annals of Applied Biology © 2012 Association of Applied Biologists
C. Feller et al. Growth stages of Asparagus officinalis according to the BBCH scale

aboveground stems are much branched and reach a Secondary stages add extra details to the principal
height from 100 cm up to more than 200 cm. The ‘leaves’ growth stages, such as the precise start and end points, to
are in fact needle-like phylloclades or cladodes in the axils assist management operations in the respective principal
of scale leaves on the stem and side shoots of all orders. growth stage. These secondary stages are also coded by
Phylloclades are 6–32 mm long, about 1 mm broad and using the numbers 0–9, which can represent an ordinal
clustered together in whorls of 2–15 phylloclades. number or a percentage, depending on the growth phase
Morphologically, asparagus belongs to the group of of the asparagus plant. The combination of the numbers
root succulents, featuring fleshy storage organs. The for the principal growth stage in the first position and
horizontally growing rhizome is a plagiotrophic growing the secondary stages in the second position results in a
stem axis with extremely short internodes and develops two-digit code.
in a sympodial manner.
Currently, vegetable asparagus is cultivated in about
62 countries worldwide with an estimated yield of 760 Growth stages of the asparagus plant
thousand tons per year and a total cultivated area of Principal growth stage 0: germination/sprouting
about 196 thousand hectares. Of this area, 35.5% are
located in Asia, 29% in Europe and 34% in North and According to the principles of the BBCH system,
South America (Benson, 2009). In America, mainly the germination of the seed and sprouting of perennial crops
young unexpanded green shoots are consumed, whereas are analogous growth stages (Hack et al., 1992) and
in western European countries white asparagus spears coded in the principal growth stage 0 (BBCH 01–09).
are preferred (Benson, 2009). White or green spears can The development of an asparagus plant originating from
be received from the same plant but some cultivars are a seed starts in the principal growth stage ‘germination’
better suited for green and others for white asparagus (BBCH 0) with stage BBCH 00 ‘dormant seed’, and ends
production. The production of green and white asparagus with ‘emergence’ when the primary shoot tip breaks
spears is determined by the cultivation method. Shoots through the soil surface (BBCH 09).
The dormant rhizome is coded BBCH 00 regardless of
turn green as soon as they break through the soil surface.
how dormancy was induced. In regions with temperate
Consequently, if white asparagus is to be produced, the
climate, dormancy is induced by low temperatures.
shoots have to be protected against light – traditionally
In tropical regions without cold-induced dormancy,
by forming soil ridges over the plants rows.
asparagus plants start a new growth cycle after the fern
The plant development is influenced by climatic
has been cut and removed from the field. In desert regions
conditions, with radiation and temperature being the
like the Peruvian cultivation area, where asparagus is
most important factors (Wilson et al., 2002), and by
cultivated via drip irrigation, growers use a drought-
management practices (e.g. harvesting).
induced dormancy. In tropical as well as in desert regions,
asparagus can be grown in a 6-month cycle and harvested
twice a year (Krarup, 1996), in contrast to the annual
Organisation of the scale
harvest in temperate regions.
The entire developmental cycle of A. officinalis, as in For white spear production, soil ridges are formed
all BBCH descriptions of plants, is subdivided into when plants are in BBCH 00. In regions with temperate
clearly recognisable and distinguishable developmental climate, this occurs at the end of winter or in early spring,
phases. These principal growth stages are described using when the soil has reached a temperature between 6◦ C
numbers from 0 to 9 in ascending order. However, and 10◦ C. In regions with warmer climate, it occurs at
principal growth stage 4 (development of harvestable the end of an induced dormancy, when the first shoot is
vegetative plant parts) is not applicable as harvest starting to grow (BBCH 01, Fig. 1, no. 01). These ridges
proceeds in principal growth stage 0 or 3. can be covered with different types of clear and coloured
If two or more principal growth stages proceed plastic films to regulate the temperature in the ridge and
simultaneously, both can be indicated by using a diagonal thus the harvesting time. Positive side effects of the cover
slash. If only one stage is to be recorded, either the are reduced problems with weeds on the ridge as well as
more advanced growth stage or the principal growth minor problems with pests like root flies. At the end of
stage of particular interest can be chosen. The principal the white asparagus harvest, either the whole ridges or
growth stages alone are not sufficient to precisely define just the sides are flattened to facilitate fern growth.
management or evaluation dates, as they only describe The next important growth stage after the subterranean
phenological events during the course of asparagus development is BBCH 09 (Fig. 1, no. 09), when the shoots
development. break through the soil surface. Following conventional

Ann Appl Biol 160 (2012) 174–180 © 2012 The Authors 175
Annals of Applied Biology © 2012 Association of Applied Biologists
Growth stages of Asparagus officinalis according to the BBCH scale C. Feller et al.

Principal growth stage 1: development of the seedling


Principal growth stage 1 (BBCH 11−19) describes the
development of asparagus seedlings in the first year only.
It is important for breeders and producers of transplants
and seedlings. The secondary stages correspond to the
respective ordinal numbers of shoots: a separation of
phylloclades developing on the new shoot signifies the
emergence of a new secondary growth stage. The primary
shoots of the seedling are restricted in their growth and
usually attain a height of only 10–20 cm (Blasberg, 1932).
The first one or two shoots form no branches. The third
and all following shoots of the seedling usually develop
branches and grow up to a height of more than 60 cm.
A seedling develops 5–6 shoots on average, although a
maximum of 10 shoots is possible.
In some areas in the world and in new cropping systems
in Germany, seedlings are propagated in peat pots in the
greenhouse for some weeks and transplanted directly in
the field at the final intrarow spacing (BBCH 13). The
intention is to avoid root damage, which may occur on
older transplants during the transplanting process.

Principal growth stage 2: formation of side shoots


(>5 cm)
The development of side shoots is relevant to the
description of the aboveground development of the
Figure 1 Principal growth stages 0 and 2: the rootstock of an asparagus asparagus plant, especially during the first years after
plant (01), a shoot breaking the soil surface (09) and the formation of side planting, when the plant does not reach its final height.
shoots (22). Initially, side shoots and inflorescence buds are becoming
visible in the axils of the scale leaves on the stem.
cultivation methods for white asparagus, spears that are Phylloclades and side shoots of higher order appear a
reaching and breaking the soil surface are continuously few days later.
harvested by manual cutting. This harvest lasts several Principal growth stage 2 (BBCH 21–29) differs from
weeks but should not exceed 10 weeks (cold-induced that of other BBCH scales. Usually, shoot development is
dormancy) and 4–6 weeks (tropical regions) to ensure classified from one to nine, with every secondary stage
that enough shoots are left to replenish the root reserves indicating the development of one side shoot. In the
for the following growing cycle (Dufault & Ward, 2005). case of asparagus, this classification is not applicable, as
However, only older crops (after three growing cycles) mostly more than nine side shoots develop in a quite
are harvested for this prolonged time in practice, whereas short time. Thus, secondary growth stage 29 would be
the harvesting period for younger plants should be reached too quickly. Hence, the development of the plant
substantially shorter. could not be described precisely enough, as principal
Nowadays, different forms of selective or full mechan- growth stage 2 shall provide a measure for the density
ical harvesting of white asparagus are used or under of the canopy. Some cultivation methods such as the
investigation (Clary et al., 2007; Cembali et al., 2008). An application of pesticides depend on the density of the
unselective full harvesting method is to lift up the ridge, canopy.
cut off all shoots and replace the ridge again within one In the following, the number of side shoots (>5 cm)
working step. In this case, the asparagus plant is reset to that are covered by the proposed scale ranges from 1
BBCH 06 after each mechanical harvest, since all growing to more than 40, categorised into groups of five shoots.
shoots are cut off. The next harvest begins when most of Hence, growth stage 21 indicates between 0 and 5 side
the shoots have reached BBCH 09 again. Depending on shoots, growth stage 22 between 6 and 10 side shoots
the plant variety and growing conditions, this method of (Fig. 1, no. 22), growth stage 23 between 11 and 15 side
harvesting can be conducted up to six times per year. shoots and so forth. Finally, growth stage 29 describes

176 Ann Appl Biol 160 (2012) 174–180 © 2012 The Authors
Annals of Applied Biology © 2012 Association of Applied Biologists
C. Feller et al. Growth stages of Asparagus officinalis according to the BBCH scale

all states with more than 40 side shoots. At each time, used as a criterion in various cultivation methods. For
the side shoots should be counted at the stem with the instance, considering fertilizer or pesticide applications,
most developed side shoots. The formation of side shoots the maximal height for common tractor passage is
runs concurrently with plant stem elongation (principal 80–90 cm. The aboveground length of the asparagus
growth stage 3). stem is given in centimetres (cm) measured from the
soil surface.
Principal growth stage 3: stem elongation

Principal growth stage 3 (BBCH 31–39) describes Principal growth stage 5: inflorescence emergence
stem elongation of the longest shoot, which is not
Flower bud development occurs axillary at the bottom
necessarily the first shoot growing aboveground. Usually,
of the scale leaves (Fig. 2, no. 51). The stretching of the
the secondary stages within principal growth stage 3
flower pedicles starts to occur before the phylloclades or
are given in percent of the typical maximum plant
side shoots are completely developed (Fig. 3, no. 55).
height/shoot length (Hack et al., 1992). This principle
In BBCH 59, the first petals are visible but flowers are
is not suitable for vegetable asparagus since length
still closed (Fig. 3, no. 59). One-year-old crops sometimes
development has a determining influence on the harvest
develop no inflorescences. The climatic conditions are of
of green asparagus. Instead, small developmental steps are
minor importance for flower formation though they have
described between BBCH 31 and BBCH 33, which allows a
a decisive effect on the lifetime and the quality of the
more accurate prediction of the appropriate harvest time.
flowers.
Green asparagus is harvested for several weeks at stage
BBCH 33. During the harvest period, many shoots grow
simultaneously from different bud clusters (Fig. 2, no.
Principal growth stage 6: flowering
32). At the time when these young unexpanded shoots
(green spears) reach a length of 20–30 cm, all of them In growth stage BBCH 60, the first flowers open
are cut close to the soil surface. The only exception is the sporadically but real flowering starts at growth stage
so-called mother fern method or mother stalk method BBCH 61 (Fig. 3, no. 61) when about 10% of the flowers
(Orton & Garrison, 2008). Here, a couple of mature have opened. The flowers are bell-shaped, greenish-white
photosynthesising shoots remain, while newly developed to yellowish, 4.5–6.5 mm long and consist of six petals
spears are harvested. partially fused together at the base. They appear singly or
After the end of the harvest period of white (BBCH in clusters of two to three flowers at the junctions of the
09) or green (BBCH 33) asparagus, the following spears branchlets. Asparagus is pollinated by insects. The flower
are allowed to complete their growth. Knowledge of is very attractive to bees (Delaplane & Mayer, 2000).
the length of the shoots is necessary because it is

Principal growth stage 7: development of fruit

Three to four days after pollination of the flower, the


ovary becomes visible. Subsequently, the ovary grows
over a period of about 3 weeks into a well-developed,
green, round-shaped berry. The berries have an average
size of 6 mm in diameter and contain two to four seeds.

Principal growth stage 8: fruit ripening

Principal growth stage 8 encompasses the discolouration


of the berries, which are green at the beginning and
turn dark red shortly before they burst (Fig. 3, no. 87).
The development of berries is important for asparagus
breeding and seed production. After berry development,
it takes about 5 weeks to ripen, altogether about 8 weeks
between pollination and formation of a ripe berry in a
Figure 2 Principal growth stages 3 and 5: stem elongation of the temperate climate. Only the seeds in a red (ripe) berry
asparagus plant (32) and stem with first inflorescences (51). are able to germinate properly.

Ann Appl Biol 160 (2012) 174–180 © 2012 The Authors 177
Annals of Applied Biology © 2012 Association of Applied Biologists
Growth stages of Asparagus officinalis according to the BBCH scale C. Feller et al.

Figure 3 Principal growth stages 5, 6 and 8: first pedicles clearly stretched (55), first flower petals visible (59), beginning of flowering (61) and ripe
fruits (87).

Principal growth stage 9: senescence, beginning 08 Stem: Shoots just before breaking the soil surface
of dormancy 09 Stem: Shoots breaking the soil surface
Seed: Emergence; primary shoot breaks through
The end of the growth cycle is described by the late
the soil surface
developmental stages BBCH 91–97. Discolouration of
plant parts progresses from green to yellow, indicating
die off of the ferns. BBCH stages 91–93 describe the Principal growth stage 1: development of the seedling
discolouration of phylloclades, stage 95 the discolouration
of the side shoots and stems. At stage BBCH 97, all 11 First phylloclade completely separated on the first
aboveground parts of the plant are dead and can be cut off. shoot
12 First phylloclade completely separated on the
The extended BBCH scale of asparagus plant second shoot
13 First phylloclade completely separated on the third
Principal growth stage 0: germination/sprouting/yield shoot
of white asparagus
1X First phylloclade completely separated on the xth
00 Stem: Dormancy of the rootstock shoot
Seed: Dry seed 19 First phylloclade completely separated on the ninth
01 Stem: First shoot just visible (<5 mm) shoot (and above)
Seed: Beginning of seed swelling; radicle not visible
03 Seed: End of seed imbibition Principal growth stage 2: formation of side shoots
05 Seed: Radicle emerged from seed (>5 cm)
06 Stem: Beginning of shoot growth (>5 mm)
Seed: Elongation of radicle, formation of root hairs 21 1–5 side shoots
and/or lateral roots 22 6–10 side shoots
07 Stem: Shoots grow to the soil surface 23 11–15 side shoots
Seed: Tip of the plant breaking the seed coat 24 16–20 side shoots

178 Ann Appl Biol 160 (2012) 174–180 © 2012 The Authors
Annals of Applied Biology © 2012 Association of Applied Biologists
C. Feller et al. Growth stages of Asparagus officinalis according to the BBCH scale

25 21–25 side shoots Principal growth stage 9: senescence, beginning of


26 26–30 side shoots dormancy
27 31–35 side shoots
28 36–40 side shoots 91 10% of the phylloclades are discoloured
29 More than 40 side shoots (yellowish)
92 50% of the phylloclades are discoloured
(yellowish)
Principal growth stage 3: stem elongation 93 All phylloclades are yellow and fallen down
95 Side shoots are discoloured
31 Longest shoot up to 10 cm long 97 Plants parts above ground are dead
32 Longest shoot up to 20 cm long
33 Longest shoot up to 30 cm long (harvest of green Conclusion
asparagus)
34 Longest shoot up to 40 cm long The proposed extended BBCH scale with its two-digit code
35 Longest shoot up to 80 cm long allows the identification of the principal growth stages
36 Longest shoot up to 120 cm long and their respective secondary stages of edible asparagus.
37 Longest shoot up to 160 cm long This code can support asparagus growers, breeders and
38 Longest shoot up to 200 cm long researchers in efficient planning of both management
39 Elongation growth of the longest shoot is ceased practices and experimental design.

Acknowledgements
Principal growth stage 5: inflorescence emergence
The authors thank the artist Mr Ernst Halwass for
51 First inflorescence or flower buds visible the creation of the drawings, and Uwe Meier, Dieter
55 First pedicles clearly stretched (first phylloclades Weber and Frank Uwihs for their discussions and helpful
are visible) comments.
59 First petals visible; flowers still closed
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Annals of Applied Biology © 2012 Association of Applied Biologists

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