Original Article

TOWARDS IMPROVED UNDERSTANDING OF SHEPARD IRREGULAR BEARING ON THE ATHERTON

TABLELANDS OF NORTH QUEENSLAND, AUSTRALIA

P. O’Farrell 1, G. Dickinson 1, B. Carr 2, C. Wright 1, E.Faichney 1, S. Newett 2

1
. Department of Agriculture and Fisheries, Mareeba, Queensland, Australia
2
. Department of Agriculture and Fisheries, Nambour, Queensland, Australia

ABSTRACT

Inconsistent yields due to irregular bearing (IB) of ‘Shepard’ avocado causes financial issues for
growers on the Atherton Tablelands in North Queensland, Australia, where this variety accounts for
53% of the region’s 2,200 ha of avocados.

Low temperatures during flowering and fruit-set are believed to be a cause of IB in ‘Shepard’. B type
flowering varieties like ‘Shepard’ are reputedly more sensitive than A type varieties such as ‘Hass’ to
low temperature influence on flower behaviour and fruit-set.

Studies were done to understand the effects of temperature on ‘Shepard’ flowering that could lead
to IB, and to evaluate ‘Hass’ as a polliniser to improve ‘Shepard’ yield consistency. Temperature,
flowering and insect activity were recorded for each variety at sites of different elevations (510, 585
and 750 m ASL) during three flowering seasons (2015‒2017).

Female and male flower stages opened later in the day at the cooler higher elevation site. This
resulted in concurrence of ‘Shepard’ stages around mid to late afternoon by which time pollinator
activity had declined.

‘Hass’ females were present in the morning when pollinators were most active on ‘Shepard’ males.
The reverse response occurred in the afternoon. Inter-planting might therefore benefit yield of both
varieties. The benefit to ‘Shepard’ could decrease if cool conditions reduced exposure of females to
pollinators active on ‘Hass’.

Practices that promote light and warmth within established ‘Shepard’ orchards could advance
daytime flower opening and improve the likelihood of female and male stages concurring earlier in
the afternoon when pollinators are more active.

Key words: avocado, flowering behaviour, honey bee, inconsistent yields, pollinisers.

INTRODUCTION

Avocado (Persea americana Mill.) is a significant crop on the Atherton Tablelands of North
Queensland, Australia, contributing 15% of the region’s gross agricultural income ($552M) in 2015
(Atherton; 17° 16’S, 145° 29’E). ‘Hass’ and ‘Shepard’ are the main varieties grown in the region with
‘Shepard’ accounting for 53% of the region’s 2,200 ha of avocados as well as representing the largest
production area of the variety in Australia.

‘Hass’, an A type flowering variety, is mainly grown on the more elevated areas around Atherton and
up to Ravenshoe (750‒1050 m ASL); and Shepard, a B type, in the less elevated and generally
warmer Mareeba‒Dimbulah area (400‒550 m ASL). Both varieties are grown in the mid-elevation
Walkamin area (550‒700 m ASL). ‘Shepard’ fruit mature on the Atherton Tablelands in February–
April when, because of early regional seasonality, avocados are in high market demand. ‘Hass’
mature in March–May.

Irregular bearing, a condition characterised by good flowering, but poor fruit-set, can affect
‘Shepard’ in lower elevated areas of Mareeba‒Dimbulah, and at Walkamin and Tolga. This leads to
inconsistent annual fruit yields, which creates financial and marketing issues for growers and fruit
handlers, and also difficulties with maintaining market share. In some years, substantial fruit-set in
local ‘Shepard’ orchards may only occur towards the end of flowering when temperatures are
seasonally higher (September–October).

Low temperatures during flowering and fruit-set are believed to be the most common cause of IB in
‘Shepard’. Disruption of avocado floral cycles by low temperatures (typically, delayed flower
opening) is well known (Davenport, 1986). B type varieties are apparently more sensitive than A
types (Sedgley and Grant, 1983). Low temperature effects that could compromise fruit-set have
been demonstrated; for example, temperature mediated changes to the floral cycle of ‘Fuerte’ (B
type) in growth-cabinets (17°C day, 12°C night) resulted in reduced pollen tube growth and no
fertilisation (Sedgley, 1977).

The flowering nature of the avocado’s perfect flower is synchronously dichogamous, and this
provides opportunities for cross pollination between A and B type varieties (Davenport, 1986).
Flowers open first as functional females, close, and then open the following day as functional males.
Because of the different floral rhythms of each type, A type females and B type males will be seen in
the morning (pollen transfer B to A), and A type males and B type females in the afternoon (pollen
transfer A to B) (Stout, 1923). While there is anecdotal evidence of improved fruit-set on trees in
adjacent rows of ‘Shepard’ and ‘Hass’ in local orchards, the long-held view of yield improvements by
inter-planting complementary varieties (i.e. ‘polliniser affect’) is inconclusive (Alcaraz and Hormaza,
2009).

This study was undertaken to gain understandings of the influence of temperature on ‘Shepard’
floral behaviour that could lead to IB, and to explore opportunities to utilise ‘Hass’ as a polliniser to
improve ‘Shepard’ yield consistency.

MATERIALS AND METHODS

Ambient temperature, flowering characteristics and insect activity associated with flowers were
recorded over three years (2015‒2017) at orchard sites on the Atherton Tablelands growing
‘Shepard’ and ‘Hass’. The sites were at Mareeba (510 m ASL), Walkamin (585 m ASL) and Tolga (750
m ASL) and described different avocado production environments as influenced by climate and soil.
Data from the Walkamin site were only collected in 2016 and 2017.

Depending on site, the study trees varied in age from 8 to 10 years. They were growing in
hedgerows at spacings ranging from 6 to 9 m within rows, and 11 to 13 m between rows. Canopies
were 5 to 7 m high and wide. Trees were in good health and flowered well each year of the study.
Hives of European honey bee (Apis mullifera), a widely accepted pollinator of avocado (Evans and
Goodwin, 2011), were present at all sites to promote pollination.

Temperature was recorded at each site at half-hourly intervals within a Stevenson screen over the
period of flowering. Mean maximum and minimum temperatures were calculated from daily
maximum and minimums. ‘Frequency of Non-Exceedance’ was calculated from minimum
temperatures for both varieties; the vertical axis of Figure 1 (describing ‘Shepard’ only) represents
the percentage of days during flowering a particular temperature was not exceeded. Potential
‘pollination’ events during flowering were also calculated from minimum temperatures. An event is
defined as a period when temperatures are potentially favourable for fruit-set and was taken as
three consecutive nights when minimums were above the thresholds of 10°C for ‘Hass’ and 13°C for
‘Shepard’. The calculated number was expressed as a percent of the total number possible during
flowering if temperatures were always above the thresholds (Table 2).

Relative flowering intensity was assessed weekly over the period of flowering. Intensity was
described on a scale from 0 (nil flowering) to 5 (full flowering). Flower gender stages (whether
female or male) were recorded during the main period of flowering, three times daily between 8:00
and 17:30 h on two days each week. Recordings were made in the morning, middle of the day and
afternoon; the interval between recordings was 2.5 to 3 hours. The order of site visits was
randomised each day. Records were taken on 10 days in 2016 and 8 days in 2017. Mean timings of
flower gender occurrence were calculated from actual observed timings (Table 3). The frequency of
gender occurrence through the day was described by the sum of actual observed timings collated to
the nearest half-hour (Figures 3 and 4).

The activity of insects foraging flowers (potential pollinators) were recorded at the same time as
flower gender. Overall activity was recorded on a scale from 0 (no insects) to 3 (> 4 insects per tree).
Total activity for each 1.5 h period through the day were averaged across years within sites, then
averaged across sites (Figure 5).

RESULTS

Maximum and minimum temperatures

Maximum and minimum temperatures during flowering generally reflected site elevation that
increases from Mareeba to Tolga (Table 1). Daily maximums and minimums at Mareeba were
commonly 2‒3°C higher than those at Tolga. Maximum temperatures at Walkamin were generally
intermediate between those of Mareeba and Tolga; however, minimum temperatures at this site
were frequently equivalent to or higher than Mareeba. Temperatures during flowering were
warmer in 2016 compared with 2015 and 2017.

(Table 1)

Indicative ‘pollination’ thresholds and events

The frequency that minimum temperatures were at or below the indicative ‘pollination’ threshold of
‘Shepard’ was lower at Mareeba compared with Tolga (Figure 1). For example, at Mareeba in 2015,
the threshold of 13°C was not exceeded on 18% of the flowering days. This compares with 47% of
flowering days at Tolga, and directly reflects the cooler temperatures of this site. In 2016 and 2017,
the percentage of times the threshold temperature was not exceeded at Walkamin was similar to
Mareeba. Differences in frequencies for ‘Hass’ (10°C threshold) across sites and years followed
similar patterns to ‘Shepard’ (data not presented). In general, the percentage of non-exceedance for
any given temperature was lower in 2016 compared with 2015 and 2017 for both varieties due to
warmer temperatures during flowering in 2016.

(Figure 1)

‘Pollination’ events reflected trends shown by ‘Frequencies of Non-Exceedance’ across sites (Table
2). The number of events as a percentage of total potential number during ‘Shepard’ and ‘Hass’
flowering was higher at Mareeba than at Tolga in all years. Over the three years, the number of
events during ‘Shepard’ flowering at Mareeba was, on average, 74% of the potential number, twice
that of Tolga.

(Table 2)

Flowering, and flower behaviour

Depending on site and year, ‘Shepard’ flowering began late June‒July, on average five weeks earlier
than ‘Hass’. Flowering of both varieties concluded at a similar time (early-mid October), resulting in
an average seven-week concurrence across sites and years (Figure 2). The period of concurrence at
Tolga, as with other sites, extended through September and early-mid October when temperatures
were more frequently above the indicative ‘pollination’ threshold of ‘Shepard’.

(Figure 2)

At all sites, ‘Shepard’ male flowers were present throughout the day (Figure 3). At Tolga, their
presence tending later into the afternoon than at the other sites (Table 3). Female flowers were
usually present from early afternoon, their earliest appearance tending later at Tolga. As a
consequence, female and male concurrence at Tolga was later in the afternoon than at the other
sites. Across sites and years, concurrence was mostly observed between 14:00 and 17:00 h.

(Figure 3)

(Table 3)

The order of ‘Hass’ female and male flower occurrence was the reverse of ‘Shepard’ (Figure 4). Like
‘Shepard’, their occurrence at Tolga was later in the day than at Walkamin and Mareeba; females
were present, and the appearance of males was later causing later female and male concurrence
(Table 3). Across sites and years, concurrence was mostly observed between 11:00 to 14:00 h,
earlier in the day than ‘Shepard’.

(Figure 4)

Pollinator activity

European honey bee was the most frequently observed insect foraging flowers at sites each year.
Other insects observed included native bee (Tetragonula sp.), and various species of fly, ants, wasps,
butterflies, lady bugs, and beetles. Apart from Tolga in 2016, foraging of ‘Shepard’ flowers during
the day tended highest in the morning around 9:45 to 11:15 h (Figure 5). In contrast, foraging of
‘Hass’ flowers tended highest in the afternoon around 14:15 to 15:45 h. These times of higher
activity were associated with the presence of male flowers of each variety. Apart from ‘Shepard’ at
Tolga in 2017, activity declined rapidly after 15:45 h.

(Figure 5)

DISCUSSION

Under the different temperature conditions of the three study sites, the general pattern of ‘Hass’
and ‘Shepard’ flower behaviour was consistent with the behaviour of A and B type varieties as
described by Stout (1923). Female flowers of ‘Hass’, an A type variety, were present in the morning
and males in the afternoon, while the gender order of ‘Shepard’, a B type variety, was the reverse.

Concurrence of female and male flowers when close pollination (Peterson, 1955) might occur, was
observed for both varieties at all sites. Across sites and years, the earliest and latest observed
timings for ‘Hass’ were 11:00 and 14:00 h, respectively, and those for ‘Shepard’ were 14:00 and
17:00 h, respectively. The frequency of recordings during the day at sites was insufficient to define
the duration of concurrence. Durations ranging from 1 to 3 hours have been reported in Israel (Ish-
Am and Eisikowitch, 1991) and Spain (Alcaraz and Hormaza, 2009).

Flower behaviour of ‘Hass’ and ‘Shepard’ was altered by temperature, a widely reported
phenomenon of other A and B type varieties (Davenport, 1986). Delayed flower timings at Tolga
meant that concurrence of female and male flowers of both varieties was later in the day than at the
warmer Walkamin and Mareeba sites. This response has not been recorded previously on the
Atherton Tablelands. For ‘Shepard’, concurrence at Tolga (mean timing 15:49 h) was at least an hour
later than at Mareeba, potentially predisposing flowers to reduced pollination opportunities. Other
limitations to pollination might also operate. For example, Ish-Am and Eisikowitch (1991) suggested
that close pollination conditions were less favourable for B type varieties compared with A type
because, unlike B type, A type females are present when fresh pollen is released from newly opened
males.

Whether low temperatures are influential in other aspects of fruit-set (pollen tube growth and
fertilisation; Sedgley, 1977) that might lead to IR at Tolga, is uncertain. Comparisons made in this
study between Tolga and Mareeba based on indicative temperature thresholds for fruit-set favoured
Mareeba (lower frequencies of non-exceedance, higher numbers of ‘pollination’ events), an area
where ‘Shepard’ has traditionally been grown because of greater yield reliability. However, while
these comparisons demonstrate that Mareeba is a warmer site, they do not clarify the involvement
of temperature in IB. More detailed studies relating temperature, floral behaviour, pollination and
fruit-set would be required to resolve this.

Prospects for improving ‘Shepard’ yield in cooler areas by inter-planting ‘Shepard’ and ‘Hass’, and
thus exploit the complementary nature of each variety’s flowering cycles, are speculative. The
relationship might prove mutually beneficial because females of each variety are present when
pollinators associated with the other’s male flowers are most active. Under cool conditions
however, the benefit to ‘Shepard’ could decrease if ‘Shepard’ female opening is delayed and females
are less exposed to pollinators active on ‘Hass’ males. Higher seasonal temperatures towards the
end of flowering (September–October; Figure 2), might advance ‘Shepard’ female opening times to
mid-afternoon when ‘Hass’ pollinators are most active, and so provide conditions more favourable
for fruit-set. This possibility is consistent with reports of improved fruit-set in local ‘Shepard’
orchards during warmer conditions at the end of flowering.

In the absence of a more reliable variety (low temperature tolerance) having similar ‘early-season’
maturity as ‘Shepard’, avocado growers have no alternative but to consider ways to mitigate IB
occurrence. Depending on circumstances, whether proposed or established orchards susceptible to
IB occurrence, growers should assess IB risk, select appropriate varieties, and use planting designs
(row orientation and spacing) and pruning practices that promote light and warmth within orchards
to improve the likelihood of female and male flower concurrence earlier in the afternoon when
pollinators are more active.

ACKNOWLEDGEMENTS

Financial support for this research was provided by Hort Innovation using the avocado research and
development levy and contributions from the Australian Government, and by the Queensland
government through the Department of Agriculture and Fisheries Queensland. Study sites and in-
kind support were provided by Atherton Tablelands avocado growers. The authors gratefully
acknowledge these contributions.

REFERENCES

Alcaraz, M.L., and Hormaza, J.I. (2009). Selection of potential pollinizers for ‘Hass’ avocado based on
flowering time and male–female overlapping. Sci. Hortic. 121, 267–271.

Davenport, T.L. (1986). Avocado flowering. Hortic. Rev. 8, 257–289.

Evans, L.J., and Goodwin, M.R. (2011). The role of insect pollinators in avocado (Persea americana)
pollination in New Zealand and Australia. Paper presented at VII World Avocado Congress (Cairns,
Australia).

Ish-Am, G., and Eisikowitch, D. (1991). New insight into avocado flowering in relation to its
pollination. Calif. Avocado Soc. Yrbk. 75, 125–137.

Peterson, P.A. (1955). Avocado flower pollination and fruit set. Calif. Avocado Soc. Yrbk. 39, 163–
169.

Sedgley, M. (1977). The effect of temperature on floral behaviour, pollen tube growth and fruit set in
the avocado. J. Hortic. Sci. 52, 135–141.
Sedgley, M., and Grant, W.J.R. (1983). Effect of low temperatures during flowering on floral cycle and
pollen tube growth in nine avocado cultivars. Sci. Hortic. 18, 207–213.

Stout, A.B. (1923). A study in cross-pollination of avocados in southern California. Calif. Avocado
Soc. Yrbk. 7, 29–45.
Table 1. Mean maximum and minimum temperatures during ‘Shepard’ and ‘Hass’ flowering.

Site Elevation ASL (m) 2015 2016 2017

Max. Min. Max. Min. Max. Min.
‘Shepard’
Mareeba 510 27.7 14.4 28.8 15.6 27.7 15.1
Walkamin 585 28.0 15.8 26.3 15.0
Tolga 750 23.8 12.1 25.7 14.2 25.7 12.7

‘Hass’
Mareeba 28.4 14.9 29.6 15.9 28.0 14.5
Walkamin 29.4 16.2 26.6 13.8
Tolga 24.6 13.2 27.6 14.8 26.3 12.0
 Mareeba Tolga

Figure 1. Minimum temperature frequencies during ‘Shepard’ flowering at Mareeba and Tolga in
relation to the variety’s indicative ‘pollination’ threshold (13°C). Vertical lines describe the indicative
‘pollination’ threshold.
Table 2. Number of ‘pollination’ events as a percentage of total potential number during flowering.
Data in parentheses describe the duration of flowering in weeks.

Site 2015 2016 2017

‘Shepard’
Mareeba 69 (12.9) 85 (11.0) 68 (15.4)
Walkamin 92 (11.0) 71 (16.3)
Tolga 29 (14.9) 44 (11.0) 30 (13.0)

‘Hass’
Mareeba 96 (6.9) 100 (9.1) 100 (10.1)
Walkamin 100 (8.1) 93 (6.1)
Tolga 89 (7.0) 85 (7.1) 62 (8.1)
Figure 2. Relative timings of ‘Shepard’ and ‘Hass’ flowering in relation to temperature as exemplified
by flowering at Tolga in 2017.
Figure 3. Frequency of occurrence of ‘Shepard’ female (♀) and male (♂) flower stages during the day
at Mareeba and Tolga. Black bars describe times when both female and male flower stages were
present (♀♂).
Table 3. Mean recorded timings of ‘Shepard’ and ‘Hass’ female (♀) and male (♂) flower stages in
2016 and 2017.

Site Mean Range Mean Range Mean Range

‘Shepard’ Latest afternoon ♂ Earliest afternoon ♀ ♂ and ♀ together
Mareeba 14:24 12:57-16:13 15:06 13:10-17:03 14:44 13:10-16:13
Walkamin 14:36 12:20-17:13 15:01 12:50-17:51 14:56 13:30-17:13
Tolga 15:32 13:00-17:15 15:47 14:50-17:15 15:49 14:50-17:15

‘Hass’ Latest afternoon ♀ Earliest ♂ ♂ and ♀ together

Mareeba 12:38 12:15-13:16 13:07 10:40-16:41 11:38 10:40-12:33
Walkamin 13:19 12:12-14:04 12:47 10:15-15:15 12:27 10:15-14:04
Tolga 13:26 12:05-16:06 13:56 10:50-17:27 13:06 10:50-16:06
Figure 4. Frequency of occurrence of ‘Hass’ female (♀) and male (♂) flower stages during the day
across three sites in 2016 and 2017. Black bars describe times when both female and male flower
stages were present (♀♂).
 40

35
Percemt of daily activity

30

25

20

15

10

0
8:15-9:45 9:45-11:15 11:15-12:45 12:45-14:15 14:15-15:45 15:45-17:15
Time during the day
Shepard Hass

Figure 5. Trends in mean activity of insects foraging ‘Shepard’ and ‘Hass’ flowers at Mareeba,
Walkamin and Tolga in 2016 and 2017. Vertical bars represent the standard error of the mean.