See discussions, stats, and author profiles for this publication at: https://www.researchgate.

net/publication/338077470

Causes of Hass Avocado Fruit Rejection in Preharvest, Harvest, and

Packinghouse: Economic Losses and Associated Variables

Article  in  Agronomy · January 2020

DOI: 10.3390/agronomy10010008

CITATIONS READS

27 5,607

3 authors:

Joaquin Guillermo Ramírez Gil Jaime Horacio López

National University of Colombia Agrosavia
156 PUBLICATIONS   640 CITATIONS    3 PUBLICATIONS   29 CITATIONS   

SEE PROFILE SEE PROFILE

Juan Camilo Henao-Rojas

Agrosavia
30 PUBLICATIONS   112 CITATIONS   

SEE PROFILE

Some of the authors of this publication are also working on these related projects:

Relation of physiopathology in post-harvest and pre-harvest variables View project

Strategies for climate adaptation in avocado View project

All content following this page was uploaded by Joaquin Guillermo Ramírez Gil on 20 December 2019.

The user has requested enhancement of the downloaded file.

Article

Causes of Hass Avocado Fruit Rejection in

Preharvest, Harvest, and Packinghouse: Economic
Losses and Associated Variables
Joaquín Guillermo Ramírez-Gil 1,*, Jaime Horacio López 2 and Juan Camilo Henao-Rojas 2
1 Departamento de Agronomía, Facultad de Ciencias Agrarias, Universidad Nacional de Colombia, 111321
Sede Bogotá, Colombia
2 Centro de Investigación La Selva-Rionegro, Corporación Colombiana de Investigación Agropecuaria-

Agrosavia, 111321 Ríonegro, Colombia; [email protected] (J.H.L.); [email protected] (J.C.H.-R.)

* Correspondence: [email protected]

Received: 27 November 2019; Accepted: 17 December 2019; Published: 19 December 2019

Abstract: The areas planted with avocado in Colombia have increased to position this fruit in
international markets. To achieve this goal, the offered fruits need to meet optimal production
standards. The aim of this study was to identify the main physiopathologies and damages that may
cause the rejection of avocado cv. Hass fruits for export purposes during pre-harvest, harvest, and
processing in packinghouses, and quantify the economic impact of said exclusion criteria.
Typological characterization and quantification of damages that may cause fruit rejection were
performed at the laboratory, field, and packinghouses. Data were obtained from 136 Colombian
productive plots with monitoring and data collection records for a minimum of five years. At the
packinghouse level, data associated with factors that affect quality (both, those identified at packing
plants and those detected in simulated shipments) were considered. The main causes of fruit
rejection during pre-harvest and harvest were: low calibers, damage to the epidermis by insect pests
from the subfamily Melolonthidae, thrips, mites, the bug Monalonion, overripe fruits, and sunburn
damage. In addition, pathologies such as anthracnose and stem end rot, and problems associated
with browning of vascular bundles, irregular ripening, chilling injury, and lenticel damage were
highly limiting at packinghouses. The economic analysis identified losses of 5.78 and 5.68% in farms
and packinghouses, respectively, which are equivalent to US dollar (USD) 80.29 per produced ton.
This work generated information that allows prioritizing strategies to improve fruit quality and
reduce economic impact.

Keywords: quality; damages; economic losses; Hass avocado

1. Introduction
Avocado (Persea americana Mill.) is a tropical species of the family Lauraceae that includes three
known races [1,2]. Different commercial varieties have originated from interspecific recombinations,
which have expanded avocado’s distribution from tropical climates to subtropical and
Mediterranean areas [3]. The Hass variety is the most cultivated worldwide and is mainly grown in
countries such as Mexico, Chile, Peru, Colombia, Indonesia, South Africa, Israel, Kenya, United
States, and Brazil [4].
Avocado in Colombia, especially the Hass variety, has shown a significant increase in planted
areas and production in recent years [5]. This growth is supported by a higher domestic demand and
the boom in exports, especially to the European Union [6]. There is currently a great expectation for
the possibility of exporting avocados to other potential markets such as Asia and the United States.

Agronomy 2020, 10, 8; doi:10.3390/agronomy10010008 www.mdpi.com/journal/agronomy

Agronomy 2020, 10, 8 2 of 13

Fruit and vegetable quality translates into nutritional, microbiological, technological,

commercial, and sensory indicators, and parameters associated with functional properties, origin,
and defects also play an important role [7]. Avocado fruit quality is achieved in crops as a result of
genetic factors, environmental conditions, agronomic management, harvest criteria, fruit selection,
and pest and disease presence, among others, and must be preserved and taken to its maximum
expression during post-harvest practices [7–12].
In Colombia, there is not enough information on quality parameters for avocado cv. Hass fruits
for export. Only a few studies about the quantity and quality of fatty acids, fruit size, extra quality
percentages, pulp yield, nutrient content and color have been reported [13–15]. Due to this situation,
Colombian fruits have obtained an average score of 5.9 out of 10 in the ranking by European quality
(6.1). These values were much lower than the ones obtained by direct competitors such as Israel (6.8),
Peru (7.1), South Africa (7.2), and Chile (7.4) [16].
Given the little information on the causes of damage that affect the external quality of avocado
cv. Hass in Colombia and the need to establish the most limiting quality parameters for avocado in
the country [16], this work had three objectives. First identify the main problems that affect the quality
of avocado cv. Hass for export during pre-harvest, harvest, and packinghouse. Second estimate the
economic impacts of said defects on the Colombian productive chain. Third identify the relationship
between environmental, topographic, and agronomics variables and incidence of rejection cause. This
research was carried out based on the records of 136 plots that export avocado in different producing
regions in Colombia and data supplied by six fruit packinghouses for export purposes.

2. Materials and Methods

2.1. Plant Material and Sampling

The data used in this study were based on the information obtained from records of 136 plots
(including 46 plots with damage characterization) that produce avocado cv. Hass and six
packinghouses from the departments of Antioquia, Caldas, Risaralda, Quindío, Tolima and Valle del
Cauca. These data were collected from a minimum of 10 harvests per plot (main and secondary).
The number of plots and packinghouses was determined based on a simple random sampling,
using the maximum variance formula (equation 1) [17]. Data provided by the Colombian Agricultural
Institute (ICA) (such as crops with registration for export and trading companies with fruit shipments
to foreign countries) were considered to determine the population. Additionally, plots that met the
following requirements were selected: (i) size greater than 4 ha, (ii) production and export history of
more than five years, and (iii) records of fruit damage and defects associated with physiopathology,
insects, mechanical factors, rodents, environmental factors, nutritional deficiencies, harvest criteria,
and size, among others. In addition, crops with environmental conditions within the ranges for
productive systems in Colombia, with locations between 1800 and 2500 m elevation, average annual
temperature between 14 and 20 °C, precipitation of 1,200–2,600 mm and relative humidity between
75 and 95% [5]. At the packinghouse level, data were related to rejections due to the aforementioned
damages, information generated in simulated shipments and the criteria of each packing company
according to the market requirements.
( )/
n= (1)
( ( )/

where:
n: sample size
N: population size
e: error range (10%)
z: value based on the confidence level (90% = 1.65)
P: probability (90%).

2.2. Characterization of Damage and Defects Associated with Pre-harvest, Harvest and Packinghouse
Processes that Affect Avocado cv. Hass Quality and Cause Fruit Rejection
Agronomy 2020, 10, 8 3 of 13

The characterization of damages that affect the external quality of Hass avocado fruits and the
identification of the origin or factor involved were possible through a detailed analysis of 46
production systems over a period of eight years (2009–2016) [11]. In each plot, fruit growth, ripening,
harvest, and transport were monitored. Problems associated with physiopathologies in the field and
packinghouse were corroborated by a polyphasic analysis at the Laboratory of “Fitotecnia Tropical”
at Universidad Nacional de Colombia, Medellín campus (Ramírez-Gil and Morales, in press).
Regarding the identification of insects and mites that affect fruits, this process was carried out at the
Francisco Luis Gutiérrez entomological museum (MEFLG) at Universidad National de Colombia,
Medellín campus. The specific identification process of each damage factor that affects the external
quality of Hass avocado fruit is described as follows:
Fruit malformations associated with boron and zinc deficiencies were identified by visual
inspection of characteristic symptomatic patterns [18,19]. In the case of damage to the fruit epidermis
caused by abiotic factors such as sunlight and hailstones, herbicide toxicity, ring-neck, and necrotic
seed that adheres to the pulp, the descriptions of these problems reported in the literature were used
as reference [20].
Regarding abiotic and biotic factors that cause disorders and pathologies that affect the external
quality of avocado at preharvest, harvest, and packinghouses such as chilling injury, fruit affected by
impacts, lenticel damage, stem end rot, anthracnose, surface cracks, scabs, and epidermis rot, their
patterns were corroborated with the information reported for each of these causes of damage [10,21–
25]. Additionally, for pathologies of biotic origin, isolation of the causal agents was performed. For
Phytophthora spp. vegetable juice culture medium (180 mL L−1), with additions of agar (24 g L−1 Difco,
Franklin Lakes, Nueva Jersey, NJ, USA), ampicillin ( 200 µg L−1), chloramphenicol (20 µg L−1), and
benlate (Benomyl ®, 100 µg L−1) (V8-AACB) were used; potato dextrose agar acidified with lactic acid
(PDA-A) (Difco, Franklin Lakes, Nueva Jersey, NJ, USA) for fungi and nutritive agar (NA) (Difco,
Franklin Lakes, Nueva Jersey, NJ, USA) supplemented with fungicide (Benomyl® 50 µg L−1) for
bacteria. Morphological characterization of fungi was performed using the keys by Barnett and
Hunter [26]. Oomycete characterization was carried out using the keys by Erwin and Ribeiro [27],
and molecular characterization was performed by amplification and sequencing of ITS regions 1, 4,
and 5 [28]. For the particular case of the isolated bacteria, basic biochemical tests were used [29]. For
each of these microorganisms, their pathogenicity on avocado fruits was confirmed.
For postharvest associated problems identified at packinghouses, simulated shipments were
performed using fruit from different plots. For these simulations, a 90% relative humidity and a
temperature of 5 ºC were established, and oxygen, carbon dioxide, and ethylene concentrations were
controlled by automated air relays and the use of ethylene absorbers in the boxes (8 g sachet). A
simulation was carried out for a period of 30 days, according to the times used in the Colombian fruit
transport chain to European markets.
For damage caused by insects or arthropods, their identification and characterization was
performed by using two approaches. The first one followed the characteristic reports that describe
damage in the field caused by insect and arthropod pests that affect Hass avocado fruits and how
they compromise quality under Colombian tropical conditions [30–33]. The second approach
consisted in the manual capture or through the use of entomological nets of individuals in plots with
high levels of insect damage and/or populations on affected structures. These individuals were
placed in jars with a 70% alcohol-sterile distilled water solution (v:v) and transported to the MELG
for identification at the genus level using taxonomic keys [30,34–40].
In the case of the damages related to malformation and lumps, changes in the epidermis color,
rounded fruits, pedicel detachment and rodents, these were identified according to the characteristics
of the damage and the origin was determined according to interviews and reports of technical
assistants at the evaluated plots. In the case of fruit size, fruit weight was used as exclusion criterion
and fruits that weighed less than 90 g were rejected [11]. Overripe fruit was associated with changes
in firmness (pre-conditioned, breaking, and firm ripe), loss of brightness and a purple to deep purple
color equivalent to the color scale between 2 and 4 according to Ochoa, [10].
Agronomy 2020, 10, 8 4 of 13

Finally, from the data obtained in the 46 plots, a detailed guide was made including the
description of symptoms and the factor or factors involved in the damages that affect the external
quality of fruits, which was shared and discussed with the technical assistants of the remaining 90
plots. With this guide, a standardization of damage reports for each crop was achieved, eliminating
those in which damage expression did not coincide. In addition, confusing reports with very low
frequencies of occurrence or without damage characterization were not taken into account.

2.3. Economic Importance Associated with Damages and Defects in Farms and Packinghouses that Generate
Fruit Selection and Rejection Criteria
The economic importance of rejected fruit was determined through a multi-step analysis [11].
This method determines the production costs of avocado crops based on their stage of development,
technological level, and production region to which they belong. In this particular case, the following
procedure was used: (i) determination of the technological level and location of the 136 evaluated
plots, (ii) production costs of one kilogram of fruit in the 136 evaluated plots according to the
technological level and production region; and (iii) determination of the economic value of fruit not
sold due to rejection factors in the field, harvest, and packinghouse according to Equations 2 and 3.
Losses were expressed in dollars per ton of produced fruit, based on an exchange rate of 1 USD: 2930
COP for Colombia.
PTD = ∑ (Pi /PT) ∗ 100 (2)
where:
PTD: total losses due to rejected fruit in %.
P: production losses due to rejection caused by factor i that affects external quality.
PT: total production of the plot according to the technological level and region where it is located.
n: amount of damage generated by fruit rejection.
i: specific damage factor that affects the external quality of fruits and generates rejection.
IEPD = PTDpc ∗ (CP) + PTDe ∗ (CP + CT + CM) (3)
where:
IEPD: economic importance of losses by fruit rejection.
PTDpc: total fruit losses due to pre-harvest and harvest rejection.
PTDe: total fruit losses due to packinghouse rejection.
CP: fruit production costs according to the technological level and location of the plot.
CT: transport cost from plot to packinghouse.
CM: cost of fruit processing in packinghouse.

2.4. Data Analysis

The incidence, origin of damage and rejection of fruits in each production system evaluated was
analyzed by means of descriptive statistics using the population mean and calculating the standard
deviation. All the analyses performed in this study, including the determination of the sampling unit,
descriptive analysis, characterization of technological levels, losses in production and economic
impact associated with rejected fruits, were carried out through the implementation of these
functions in the statistical program R version 3.6.0 [41].

2.5. Relation between Causes of Rejection and Environmental and Management Variables
The environmental variables included in the evaluation were temperature (°C), precipitation
(mm), and relative humidity (%), obtained from weather stations (WatchDog serie 2000 ™, Spectrum
Technologies, Aurora, CO, USA) located in some of the plots evaluated. Environmental data for the
plots where no stations were available, were obtained by interpolation using data from the climatic
network available at Ideam, Colombia (Institute of hydrology, meteorology and environmental
studies), using the Higher Order Delaunay Triangulations (HODTs) [42], implemented in R [41].
These variables were complemented with elevation data obtained for each avocado plot using a GPS
Agronomy 2020, 10, 8 5 of 13

equipment (Triple Serie GeoXT, Trimble Navigation Limited, Westminster, CO, USA) adjusted under
the projection system UTM WGS 84 Zone 18 N. In addition, each plot was classified in a technological
level as low, medium, and high [11].
In order to identify if there are clusters between the environmental, topographic and
management variables and the incidence of each of the rejection causes, unsupervised and supervised
grouping tools were used. This process was carried out by integrating K-means and support vector
machine algorithms implemented in R [41]. These methods were calibrated with 70% of the data and
their validation was carried out with 30% of the remaining data by the cross-validation method.

3. Results

3.1. General Description of Damages Associated with the External Quality of Hass Avocado Fruits
Avocado fruits and their external quality in the 136 evaluated plots and packinghouses were
altered by different factors, which were grouped into four clusters. In a first group, those alterations
that affected fruit shape and size were identified. Some of the factors reported in this group are:
malformations or lumps with unknown origin (Figure 1A), boron (Figure 1B), and zinc (Figure 1C)
deficiencies, very rounded fruits with unknown origin (Figure 1E), fruits with reduced size and
necrotic seed that adheres to the pulp, whose origin seems to be related to periods of fruit filling with
water deficit as a consequence of the “El niño” phenomenon (Figure 1P), and fruit malformation due
to the avocado ovary gall midge (Bruggmanniella perseae, Gagné) (Figures 2E,F).

Figure 1. Malformation, nutritional deficiencies, mechanical defects, disorders and environmental

damage affecting fruit in Hass avocado: (A) malformation of unknown origin; (B) boron deficiency;
(C) zinc deficiency; (D) natural variegation; (E) fruit shape; (F) mechanical damage; (G) fruit without
pedicel; (H) herbicide damage; (I) ring-neck; (J) impact damage; (K) sunburn damage; (L) hailstone
damage; (M–O) overripe fruit; (P) necrotic seed; (Q) lenticel damage; (R) chilling injury.

Another group of defects that affected quality was associated with factors that alter the fruit
epidermis and, to a lesser extent, the pulp. Within these factors we could find changes in the
epidermis color with unknown origin (Figure 1D), damage caused by mechanical tools (Figure 1F),
black and brown spots caused by herbicide drift and sunburn (Figure 1H and K), breaking of the
epidermis by hailstones (Figure 1L), and lenticel damage (Figure 1Q). This cluster also grouped
Agronomy 2020, 10, 8 6 of 13

damage caused by the majority of insects and arthropods that alter the epidermis, cause lumps,
induce exudates on lesions, or simply settle on the tissue. Within these arthropods there are mites
(Figure 2A) (Olygonichus yothersi Mcgregor), the Melolonthidae complex (Figure 2B) (Astaena
pigydialis Kirsch, mainly), thrips (Figure 2C) (Thysanoptera), the bug monalonion (Figure 2D)
(Monaloniun velezangeli Carvalho and Costa), and scales (Figure 3G,H) (Hemiptera: Coccoidea).
Similarly, different rodents that cause epidermis detachment and holes in the pulp were included in
this cluster (Figure 3N,O).

Figure 2. Damage caused by pests affecting fruit in Hass avocado: (A) mites (principally associated
with Olygonichus yothersi Mcgregor); (B) Melolonthidae (principally associated with Astaena pigydialis
Kirsch); (C) thrips (Thysanoptera); (D) the bug monalonion (Monaloniun velezangeli Carvalho and
Costa); (E,F) ovary gall midge (Bruggmanniella perseae Gagné); (G,H) scales (Hemiptera: Coccoidea)
(Photos: Wilmar Perez); (I–K) avocado seed moth (Stenoma catenifer Walsingham) (L,M) big avocado
seed weevil (Heilipus lauri Boheman). (N,O) rodent damage.

Physiopathologies make up another group of fruit rejection causes with a strong presence
mainly during postharvest. Some of the pathologies of abiotic origin found were the appearance of
necrotic areas in the epidermis and pulp associated with impacts (Figure 1J), irregular ripening
characterized by pulp areas with different ripening levels, adhered and pre-germinated seeds (Figure
1M,N,O) and chilling injuries with different expressions which include epidermis areas with intense
black coloration and pulp and fibers with browning and purple coloration (Figure 2R). On the other
hand, the pathologies of biotic origin were anthracnose (Colletotrichum gloeosporioides sensu lato), stem
end rot (Rhyzopus sp., Lasiodiplodia sp., Pestalotia sp., and Phomopsis sp.), avocado scab (Sphaceloma
persea Jenk), cracks in the epidermis caused by Cercospora spot (Pseudocercospora purpurea (Cooke)
Deighton), pedicel lesions (Colletotrichum gloeosporioides sensu lato, P. purpurea, S. persea, Pestalotia sp.)
and fruit epidermis rot (Rhyzopus sp., Lasiodiplodia sp., Botryosphaeria obtusa (Schwein), Dothiorella sp.,
Pestalotia sp., and Phomopsis sp.) (Figure 3).
In the last group of damages that cause immediate fruit discard we could find fruit without
pedicel (Figure 1G), ring-neck (Figure 1I), overripe fruit (Figure 1M), and fruit with damage caused
Agronomy 2020, 10, 8 7 of 13

by quarantine pests such as Stenoma catenifer Walsingham and Heilipus lauri Boheman (Figure 2I,J,K,
L, and M).

Figure 3. Symptoms of disease affectation on fruit in Hass avocado, A to D symptoms associated with
anthracnose (Colletotrichum gloeosporioides sensu lato). (A) lesion in external epidermis; (B) lesion in
internal epidermis; (C) advanced infection in external epidermis; (D) advanced infection in all
mesocarp; (E) typical symptoms associated with stem end rot caused by different microorganisms
(Rhyzopus sp., Lasiodiplodia sp., Dothiorella sp., Pestalotia sp., and Phomopsis sp.); (F) superficial cracks
caused by Pseudocercospora purpurea (Cooke) Deighton; (G) pedicel lesion caused by different
microorganisms (Colletotrichum gloeosporioides sensu lato, Pseudocercospora purpurea (Cooke) Deighton,
Sphaceloma persea Jenk, Pestalotia sp.) (Photo: Anibal Lopez); (H) scab caused by Sphaceloma persea Jenk;
(I) simultaneous infection caused by Colletotrichum gloeosporioides sensu lato and Sphaceloma persea Jenk;
(J) fruit rot caused by different microorganisms (Rhyzopus sp., Lasiodiplodia sp., Botryosphaeria obtusa
Schwein, Dothiorella sp., Pestalotia sp., and Phomopsis sp.). Causal agents and symptoms for each of the
pathologies were based on reports by Ramírez-Gil (2018).

3.2. Incidence and Rejection Associated with the Main Damages in Pre-harvest, Harvest and Packinghouse
that Affect Hass Avocado Quality
Fruit damages or alterations related to malformations, changes in color, nutritional deficiencies,
impacts, environmental conditions (hailstones, sunlight) and agronomic practices (damage by
machinery) presented different degrees of relevance, both at field and packinghouse levels. Fruit
malformations (Figure 1A) and changes in the epidermis color (Figure 1D) showed minimal
incidence, and no rejection data were reported. Regarding boron and zinc deficiencies (Figure 1B and
C) their incidence was less than 0.3%, with rejection values greater than 90% (Figures 4 and 5A). The
following fruit discard causes showed incidences below 0.5% (Figure 4): presence of very rounded
fruit shape, with rejection values between 35% and 40% in the field and packinghouse (Figures 1E
and 5A); damage caused by mechanical tools (Figures 1F and 6A), fruit without pedicel (Figures 1G
and 5A), herbicide phytotoxicity (Figures 1H and 5A), overripe fruit (Figures 1M,N,O and 5A), and
necrotic seed that adheres to the pulp (Figure 1P) all had 100% rejection; finally, epidermis damage
due to hailstones had rejection values between 15% and 35% in the field and packinghouse (Figure
1L and 5A).
Ring-neck (Figure 1I), lenticel damage (Figure 1Q) and fruit size were the most relevant fruit
discard causes especially during pre-harvest, with incidence and rejection values of 0.4–100%, 1–15%,
and 3.6–50%, respectively (Figures 4 and 5A). Regarding post-harvest, fruit quality was altered by
impacts (Figure 1J), lenticel damage (Figure 1Q), chilling injury (Figure 1R), fruit size and sunburn
damage (Figure 1k), with incidences of 0.8%, 2.4%, 1.8%, 1.5%, and 0.8%, respectively, and different
rejection percentages (between 20% and 80%) (Figure 4).
Agronomy 2020, 10, 8 8 of 13

Figure 4. Incidence and rejection of avocado Hass fruits affected with diseases, pests, malformation,
mechanical damage, disorders, and abiotic damage. Data from fields were obtained from 136 plots
planted in the departments of Antioquia, Caldas, Risaralda, Quindío, Valle, and Tolima. Data from
packinghouses were obtained from four companies. Line on bars represents the standard deviation
of data.

In the case of damages associated with insects and rodents, their relevance was not strictly
related to incidence, but with the level of fruit alteration and the restriction that some pests have as
quarantine pests. Thus, mites (Figure 2A), the Melolonthidae complex (Figure 2B) and thrips (Figure
2C) have the highest incidence with values between 1 and 2.5% (Figure 5) and rejection in the field
and packinghouse of 20–50%, 20–35%, and 10%–15.6%, respectively. Packinghouses tolerate these
damages so their discard is low. Regarding damages caused by the bug monalonion (Figure 3D) and
scales (Figures 2G,H), their incidences were less than 0.3% in the field, with 100% rejection in the field
and packinghouse since their damage is not tolerated (Figures 4 and 5A). On the other hand, data
regarding ovary gall midge (Figure 2E,F) and rodents (Figure 2N,O) incidence in the field were not
taken into account since they appear very sporadically and fruit was immediately discarded when
they were spotted. In the case of pests with quarantine restrictions, the presence of Stenoma catenifer
Walsingham (Figure 2I–K) and Heilipus lauri Boheman (Figure Land M) was sporadic and fruits and
branches were removed when they were spotted in a plot.
Pathologies such as anthracnose (Figures 3A,B,C, and D) and stem end rot (Figure E) were
highlighted in the plots studied in this work. For these pathologies, incidence and rejections of
affected fruit at packinghouses showed values of 1.3%–52.5% and 1.5%–70.1%, respectively, which
were much higher than those reported in the field (0.5%–15.3% and 0.8%-18.5%, respectively) (Figure
4 and 5A). Other pathologies with lower incidence were: avocado scab, cracks in the epidermis,
pedicel lesions, and fruit rot with incidences below 0.2%, and rejection values greater than 65 and
90% in the field and packinghouse (Figures 4 and 5A).

3.3. Economic Importance of Damages and Defects in Farms and Packinghouses that Generate Fruit Selection
and Rejection Criteria
The costs of total fruit discarded for different reasons (Figures 4 and 5A) in farms (5.78%) and
packinghouses (5.68%) were USD 80.29 per each ton of produced fruit (Figure 6 B). The following
losses are highlighted: fruit size (USD 22), the Melolonthidae complex (USD 9.25), stem end rot (USD
8.19), anthracnose (USD 5.25), lenticellosis (USD 4.76), fruit damage caused by mites (USD 3.36),
Agronomy 2020, 10, 8 9 of 13

overripe fruit (USD 2.94), sunburn damage (USD 2.93), fruit affected by impacts (USD 2.90), ring-
neck (USD 2.8), rounded fruit shape (USD 2.38) and thrips damage (2.17 USD) (Figure 5B). For the
other problems affecting fruit quality, the economic value was less than 2 USD (Figure 5B).

Figure 5. Economics loss and costs of avocado Hass fruits associated with damage caused by diseases,
pests, malformation, mechanical factors, disorders, and abiotic problems. (A) data is the sum of fruit
rejected in fields and packinghouses; (B) the cost was obtained based on equation 1. Data from fields
were obtained from 200 plots planted in the departments of Antioquia, Caldas, Risaralda, Quindío,
Valle, and Tolima. Data from packinghouses were obtained from four companies. Line on bars
represents the standard deviation of data. Losses were expressed in dollars per ton of produced fruit,
based on an exchange rate of 1 USD: 2930 COP for Colombia.

3.4. Relation between Causes of Rejection and Environmental and Management Variables
The methods of unsupervised and supervised grouping showed that the incidences of the causes
of rejection of the fruit in avocado are highly influenced by the elevation and the technological degree
of the production system, while the other variables did not allow to identify groups (Figure 6).
Agronomy 2020, 10, 8 10 of 13

Figure 6. Supervised and unsupervised clustering of the incidences of avocado rejection and
environmental, topographic, and crop management variables. Clusters were made using K-means
and support vector machine algorithms.

4. Discussion
Avocado fruits and their quality can be altered by different factors. The presence of certain
damage can only be cosmetic or can compromise fruit quality in terms of nutritional and sensory
contents. In addition, it can threaten the phytosanitary safety of the importing country. Fruit rejection
or inclusion for export purposes is determined based on damage intensity and type, and each trading
company and importing country has different exclusion or damage tolerance criteria.
Avocado fruit quality is the sum of the entire production process, which involves plant material
suppliers, producers, packers, distributors, and consumers. The synergistic relations between each of
these links in the production chain are acquiring more importance day by day [43]. That is why it is
necessary to establish clear communication channels in order to define quality standards and develop
sufficient technologies to increase quality and reduce economic losses due to discarded fruit.
Some of the quality-related problems found in this study are inappropriate harvest and post-
harvest practices since the mechanical damage generated at these stages affects the cosmetic
appearance of fruits or may be the gateway to pathogens that cause postharvest diseases. Mechanical
damage can also generate higher metabolic rates in fruits, and therefore, premature and irregular
ripening [7,12]. In addition, harvest under appropriate environmental and logistic conditions that
meet the right criteria or standards (harvest index, dry fruit, packaging, transport, etc.) will avoid
problems related to lenticellosis, high respiration rates, disease incidence, vascular browning, among
others [21,25,44].
One of the most relevant parameters that affect fruit quality identified in this study was
associated with fruit ripening for consumption. It is evident that some of the most important
challenges the Colombian Hass avocado industry has is offering consumers a healthy product with
homogeneous ripening [15,45]. This is due to the fact that avocado is a climacteric fruit whose
consumption ripening is achieved several days after its harvest [46] and its final quality depends
largely on its pre-harvest conditions [24,47,48]. This situation implies that the Colombian production
system still lacks information to identify the harvest criteria with the greatest influence on avocado
ripening processes and their effect on fruit quality and international market perception.
Damages caused by pathologies that affect fruit external and internal quality proved to be quite
limiting since their infection can occur during pre-harvest and harvest. Given their endophytic
nature, disinfection and post-harvest treatments are difficult to carry out, despite the fact that this
Agronomy 2020, 10, 8 11 of 13

type of risk can be reduced by performing an adequate ripening process (control of temperature and
relative humidity) to avoid proliferation of opportunistic organisms in fruits at consumption ripeness
[24,49,50].
It was found that the causes of avocado cv. Hass fruit rejection are highly limiting in economic
terms, leading to significant losses that affect the profitability of the production system. This implies
the need to apply management and control measures to reduce causal factors affecting quality. The
unsupervised and supervised group managed to identify how elevation is a parameter that has a
high influence on the presence of many causes of rejection. On the other hand, the technological
degree achieved a separation in groups depending on the level of incidence of the problems (high,
high, medium, and low incidence).
Author Contributions: Conceptualization, J.C.H-R., J.H.L., and J.G.R-G.; data acquisition, J.G.R-G.; data
analysis, J.G.R-G., and J.C.H-R.; design of methodology, J.G.R-G.; writing and editing, J.C.H-R., J.H.L., and J.G.R-
G. All authors have read and agreed to the published version of the manuscript.

Funding: This research received no external funding

Acknowledgments: the authors would like to thank the farm owners that allowed the collection of information
associated with the problems that affect fruit quality and their economic importance. We also thank the avocado
technical assistants who answered our call and were willing to help unselfishly with this work by sharing the
farms data and their experiences. We would also like to acknowledge the packinghouses that, for commercial
reasons, requested their names not to be included in the manuscript. This work not was financed by a specific
institution, and the cost was assumed by the authors

Conflicts of Interest: The authors declare no conflict of interest

References
1. Bregh, B.; Ellstrand, N. Taxonomy of the avocado. Calif. Avocado Soc. Yearb. 1986, 70, 135–145.
2. Chen, H.; Morrell, P.L.; Ashworth, V.E.T.M.; de la Cruz, M.; Clegg, M.T. Tracing the geographic origins of
major avocado cultivars. J. Hered. 2009, 100, 56–65.
3. Bost, J.B.; Smith, N.J.; Crane, J.H. History, distribution and uses. In The Avocado: Botany, Production and Uses,
2nd ed.; CABI Publ: Wallingford, UK, 2013; pp. 10–30.
4. FAO. FAOSTAT. Available online: http://www.fao.org/faostat/es/#home (accessed on 9 January 2019).
5. Ramírez-Gil, J. Avocado wilt complex disease, implications and management in Colombia. Rev. Fac. Nac.
Agron. Medellín 2018, 71, 8525–8541.
6. Ministerio de Agricultura y Desarrollo Rural de Colombia. Cadena de Aguacate; Indicadores e Instrumentos;
Bogotá, Colombia, 2018.
7. Bill, M.; Sivakumar, D.; Thompson, A.K.; Korsten, L. Avocado fruit quality management during the
postharvest supply chain. Food Rev. Int. 2014, 30, 169–202.
8. Ferreyra, R.; Sellés, G.; Saavedra, J.; Ortiz, J.; Zúñiga, C.; Troncoso, C.; Rivera, S.A.; González-Agüero, M.;
Defilippi, B.G. Identification of pre-harvest factors that affect fatty acid profiles of avocado fruit (Persea
americana Mill) cv. ‘Hass’ at harvest. South Afr. J. Bot. 2016, 104, 15–20.
9. Herrera-González, J.A.; Salazar-García, S.; Gutiérrez-Martínez, P.; González-Durán, I.J.L. El
comportamiento poscosecha de frutos de aguacate ‘Hass’ es influenciado por el portainjerto. Rev. Mex.
Cienc. Agríc. 2013, 4, 19–32.
10. Ochoa, S. Calidad pos-cosecha del fruto de aguacate Hass. IV Encuentro Nacional de la Cadena Productiva
del Aguacate. In Proceedings of the Encuentro Cadena de Aguacate; Politécnico Colombiano Jaime Isaza
Cadavid Medellín, Medellín, Colombia, 10 November 2012; pp. 1–30.
11. Ramírez-Gil, J.G.; Gilchrist Ramelli, E.; Morales Osorio, J.G. Economic impact of the avocado (cv. Hass) wilt
disease complex in Antioquia, Colombia, crops under different technological management levels. Crop Prot.
2017, 101, 103–115.
12. Salazar-García, S.; Medina-Carrillo, R.E.; Álvarez-Bravo, A.; Salazar-García, S.; Medina-Carrillo, R.E.;
Álvarez-Bravo, A. Evaluación inicial de algunos aspectos de calidad del fruto de aguacate ‘Hass’ producido
en tres regiones de México. Rev. Mex. Cienc. Agríc. 2016, 7, 277–289.
13. Bernal, J. Estudios Ecofisiológicos en Aguacate cv. Hass en Diferentes Ambientes Como Alternativa
Productiva en Colombia. PH.D. Thesis, Universidad Nacional de Colombia-Sede Medellín, Medellín,
Colombia, 2016.
Agronomy 2020, 10, 8 12 of 13

14. Carvalho, C.P.; Velásquez, M.A.; Rooyen, Z.V. Determination of the minimum dry matter index for the
optimum harvest of “Hass” avocado fruits in Colombia. Agron. Colomb. 2014, 32, 399–406.
15. Henao-Rojas, J.; Rodríguez, P. Evaluation of color during avocado (Persea americana Mill. cv. Hass)
ripening | Request PDF. Agron. Colomb. 2016, 31, 876–879.
16. Analdex. Los Retos del Aguacate Hass Colombiano en Los Mercados Internacionales; Analdex, Bogota, Colombia,
2017; pp. 1–29.
17. Cochran, W. Sampling Techniques, 3rd ed.; John Wiley & Sons, Inc.: New York, NY, USA, 1977.
18. Crowley, D.E.; Smith, W.; Faber, B.; Manthey, J.A. Zinc fertilization of avocado trees. HortScience 1996, 31,
224–229.
19. Whiley, A.W.; Smith, I.; Wolstenholme, B.N.; Saranah, J.B. Boron nutrition of avocados. South Afr. Avocado
Grow. Assoc. Yearb. 1996, 19, 1–7.
20. Toerien, J. Seasonal incidence of ring-neck on avocados and possible causes. South Afr. Avocado Grow. Assoc.
Res. Rep. 1979, 3, 49–51.
21. Everett, K.R.; Hallett, I.C.; Rees-George, J.; Chynoweth, R.W.; Pak, H.A. Avocado lenticel damage: The
cause and the effect on fruit quality. Postharvest Biol. Technol. 2008, 48, 383–390.
22. Ginsberg, L. Posharvest physiological problema of avodados. South Afr. Avocado Grow. Assoc. Yearb. 1985,
8, 8–11.
23. Kassim, A.; Workneh, T.; Bezuidenhout, C. A review on postharvest handling of avocado fruit. Afr. J. Agric.
Res. 2013, 8, 2385–2402.
24. Ochoa, S. Calidad y manejo pos-cosecha del fruto de aguacate. In Proceedings of the III
CongresoLatinoamericano del Aguacate, Medellín, Colombia, 24 August 2009; pp. 1–17.
25. Van Rooyen, Z. Factors Affecting Mesocarp Discolouration Severity in “Pinkerton” Avocados (Persea
Americana MILL.). Ph.D. Thesis, University of Kwazulu Natal, Pietermaritzburg, South Africa, 2005.
26. Barnett, H.L.; Hunter, B.B. Illustrated Genera of Imperfect Fungi; Burgess Publishing Company: Minneapolis,
MN, USA, 1972.
27. Erwin, D.C.; Ribeiro, O.K. Phytophthora Diseases Worldwide; American Phytopathological Society: St. Paul,
MN, USA, 1996.
28. White, T.; Bruns, T.; Lee, S.; Taylor, L. Amplification and direct sequencing of fungal ribosomal RNA genes
for phylogenetics. In PCR Protocols: A Guide to Methods and Applications; Academic Press: San Diego, CA,
USA, 1990; pp. 315–322.
29. Shaad, N.; Jones, J.; Chun, W. Laboratory Guide for Identification of Plant Pathogenic Bacteria; Schaad, N.W.,
Jones, J.B., Chun, W., Eds; American Phytopathological Society: St. Paul, MN, USA, 2001.
30. Diaz Grisales, V.; Caicedo Vallejo, A.M.; Carabalí Muñoz, A.; Diaz Grisales, V.; Caicedo Vallejo, A.M.;
Carabalí Muñoz, A. Ciclo de vida y descripción morfológica de Heilipus lauri Boheman (Coleoptera:
Curculionidae) en Colombia. Acta Zoológica Mex. 2017, 33, 231–242.
31. Londoño, M.E.; Kondo, T.; Carabali, A.; Varon, E.; Caicedo, A. Insectos y acaros. In Actualización Tecnológica y
Buenas Prácticas Agrícolas (BPA) en el Cultivo de Aguacate; CORPOICA: Antioquia, Colombia, 2014; pp. 228–283.
32. Torres-Jaimes, L.F.; Cartagena-Valenzuela, J.R.; Correa-Londoño, G.A.; Monsalve-García, D.A.; Londoño-
Zuluaga, M.E. Relación entre la presencia y el daño de Monalonion velezangeli Carvalho & Costa y algunos
factores climáticos en cultivos de aguacate cv. Hass. Cienc. Tecnol. Agropecu. 2015, 16, 79–85.
33. Valencia Arias, C.; Martínez Osorio, A.; Morales Osorio, J.G.; Ramírez-Gil, J.G. Spatial Analysis of Presence,
Injury, and Economic Impact of the Melolonthidae (Coleoptera: Scarabaeoidea) Complex in Avocado
Crops. Neotrop. Entomol. 2019, 48, 583–593.
34. Gagné, R.J.; Posada, F.; Zulma, N.G. A new species of Bruggmanniella (Diptera: Cecidomyiidae) aborting
young fruit of avocado, Persea Americana (Lauraceae), in Colombia and Costa Rica. Proc. Entomol. Soc.
Wash. 2004, 106, 547–553.
35. Krantz, G.; Walter, D. A Manual of Acarology, 3rd ed.; Texas Tech University Press: Lubbock, Texas, TX, USA,
2009.
36. Lambdin, P.; Kosztarab, M. Morphology and Systematics of the Adult Females of the Genus Cerococcus
(Homoptera: Coccoidea: Cerococcidae). In Studies on the Morphology and Systematics of Scale Insects; Virginia
Polytechnic Institute and State University: Virginia, CA, USA, 1997.
37. Morón, M.Á.; Neita-Moreno, J.C. Nuevas especies colombianas de Phyllophaga Harris (Coleoptera:
Melolonthidae: Melolonthinae). Caldasia 2014, 36, 203–216.
 Agronomy 2020, 10, 8 13 of 13

38. Mound, L.; Marrullo, R. The thrips of Central and South America: An Introduction (Insecta: Thysanoptera).
In Memories of Entomology; Associated Pub.: Liverpool, UK, 1996.
39. Soto-Rodríguez, G.A.; Rodríguez-Arrieta, J.A.; González Muñoz, C.; Cambero-Campos, J.; Retana-Salazar,
A.P.; Soto-Rodríguez, G.A.; Rodríguez-Arrieta, J.A.; González Muñoz, C.; Cambero-Campos, J.; Retana-
Salazar, A.P. Key to the identification of genera of Thrips (Insecta: Thysanoptera) commonly associated
with ornamental plants in Central America. Acta Zoológica Mex. 2017, 33, 454–463.
40. Vallejo, F.; Morón, M.A. Description of the immature stages and redescription of the adults of Ancognatha
scarabaeoides Erichson (Coleoptera: Scarabaeidae: Dynastinae), a member of the soil white grub
assemblage in Colombia. Coleopt. Bull. 2008, 62, 154–164.
41. R Development Core Team R. The R Project for Statistical Computing. Available online: https://www.r-
project.org/ (accessed on 9 June 2019).
42. Gudmundsson, J.; Hammar, M.; van Kreveld, M. Higher order delaunay triangulations. Comput. Geom.
Theory Appl. 2002, 23, 85–98.
43. Arias Bustos, C.; Moors, E.H.M. Reducing post-harvest food losses through innovative collaboration:
Insights from the Colombian and Mexican avocado supply chains. J. Clean. Prod. 2018, 199, 1020–1034.
44. Duvenhage, J. The influence of wet picking on post harvest diseases and disorders of avocado fruit. South
Afr. Avocado Grow. Assoc. Yearb. 1993, 16, 77–79.
45. Rivera, S.A.; Ferreyra, R.; Robledo, P.; Selles, G.; Arpaia, M.L.; Saavedra, J.; Defilippi, B.G. Identification of
preharvest factors determining postharvest ripening behaviors in ‘Hass’ avocado under long term storage.
Sci. Hortic. 2017, 216, 29–37.
46. Hershkovitz, V.; Friedman, H.; Goldschmidt, E.E.; Feygenberg, O.; Pesis, E. Induction of ethylene in
avocado fruit in response to chilling stress on tree. J. Plant Physiol. 2009, 166, 1855–1862.
47. Giovannoni, J. Molecular biology of fruit and maturation and ripening. Annu. Rev. Plant Physiol. Plant Mol.
Biol. 2001, 52, 725–749.
48. Seymour, G.; Tucker, G. Avocado. In Biochemistry of Fruit Ripening; Chapman and Hall: London, UK, 1993;
pp. 53–81.
49. Hartill, W.F.T.; Everett, K.R. Inoculum sources and infection pathways of pathogens causing stem-end rots
of ‘Hass’ avocado(Persea Americana). N. Z. J. Crop Hortic. Sci. 2002, 30, 249–260.
50. Sharma, G.; Maymon, M.; Freeman, S. Epidemiology, pathology and identification of Colletotrichum
including a novel species associated with avocado ( Persea americana ) anthracnose in Israel. Sci. Rep. 2017,
7, 15839, doi:10.1038/s41598-017-15946-w.

© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access
article distributed under the terms and conditions of the Creative Commons Attribution
(CC BY) license (http://creativecommons.org/licenses/by/4.0/).

View publication stats