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AGROECOLOGICAL ANALYSIS OF ARTHROPODS INVOLVED IN MANGO POLLINATION IN SOUTH FLORIDA
By
MATTHEW QUENAUDON
A THESIS PRESENTED TO THE GRADUATE SCHOOL
OF THE UNIVERSITY OF FLORIDA IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF
MASTER OF SCIENCE
UNIVERSITY OF FLORIDA
2019
© 2019 Matthew Quenaudon
To my parents
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ACKNOWLEDGMENTS
I am grateful to my major professor Dr. Daniel Carrillo, for his guidance, support,
and prowess during my time as a graduate student at the University of Florida. Dr.
Carrillo was always patient, thoughtful, and provided his insights while allowing me the
intellectual freedom to shape my own research. I also want to thank the other members
of my committee, Dr. Zachary Brym, Dr. Jonathan Crane, Dr. Rachel Mallinger, and Dr.
Catharine Mannion whose expertise and contributions greatly improved this study. I
thank Alejandra Canon and Mariane Ruviéri for their contributions to data collecting and
analyzing. Thank you to Dr. Gary Steck for his aid in the identification of insects and Dr.
Alexandra Revynthi for her statistical help. I am grateful to everyone in the Tropical Fruit
Entomology lab, including Jose Alegria, Luisa Cruz, Rita Duncan, and Octavio Menocal
who helped and created a positive work environment. Lastly, I am thankful to my family
for their support and loving encouragement, providing me the motivation and mental
fortitude to complete my study.
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TABLE OF CONTENTS page
ACKNOWLEDGMENTS .................................................................................................. 4
LIST OF TABLES ............................................................................................................ 7
LIST OF FIGURES .......................................................................................................... 8
ABSTRACT ................................................................................................................... 10
CHAPTER
1 LITERATURE REVIEW .......................................................................................... 12
Origin, Distribution, and Importance of Mangifera indica ........................................ 12
Reproductive Physiology and Floral Biology ........................................................... 14
Insect Pollinators .................................................................................................... 16 Objectives of Master of Science Thesis Research .................................................. 22
2 MOST FREQUENT ARTHROPOD VISITORS ON ‘KEITT’ MANGO (MANGIFERA INDICA) FLOWERS IN SOUTH FLORIDA ...................................... 23
Introduction ............................................................................................................. 23
Material and Methods ............................................................................................. 25
Results .................................................................................................................... 28
Order Diptera .................................................................................................... 29 Chloropidae ................................................................................................ 30
Drosophilidae ............................................................................................. 30 Sciaridae .................................................................................................... 31 Muscidae.................................................................................................... 31
Syrphidae ................................................................................................... 31 Calliphoridae .............................................................................................. 31 Ceratopogonidae ....................................................................................... 32
Order Coleoptera .............................................................................................. 32 Cryptophagidae .......................................................................................... 32 Coccinellidae .............................................................................................. 32
Curculionidae ............................................................................................. 33 Order Hemiptera ............................................................................................... 33
Miridae ....................................................................................................... 34 Cicadellidae ............................................................................................... 34
Aphididae ................................................................................................... 34 Anthocoridae .............................................................................................. 35 Other Hemiptera ........................................................................................ 35
Order Hymenoptera .......................................................................................... 35 Apidae ........................................................................................................ 36 Formicidae ................................................................................................. 36
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Eulophidae ................................................................................................. 36
Other Hymenoptera ................................................................................... 37
Order Lepidoptera ............................................................................................ 37 Order Thysanoptera ......................................................................................... 37 Order Araneae .................................................................................................. 38 Insect Dependency on Bloom Period ............................................................... 38
Discussion .............................................................................................................. 39
Pollinator Candidates Based on Population Density ........................................ 39 Differences in Orchards .................................................................................... 42
3 INSECT BEHAVIOR AND POLLEN COLLECTION DURING FLOWER VISITATIONS ......................................................................................................... 60
Introduction ............................................................................................................. 60 Materials and Methods............................................................................................ 62 Results .................................................................................................................... 64
Discussion .............................................................................................................. 68
4 IMPORTANCE OF ARTHROPODS IN POLLINATION AND FRUIT SET AND PRODUCTION OF MANGIFERA INDICA .............................................................. 76
Introduction ............................................................................................................. 76 Material and Methods ............................................................................................. 78
Results .................................................................................................................... 80 Discussion .............................................................................................................. 80
5 CONCLUDING SUMMARY ON PRIMARY INSECTS INVOLVED IN MANGO POLLINATION IN THE SOUTH-FLORIDA REGION .............................................. 94
LIST OF REFERENCES ............................................................................................... 97
BIOGRAPHICAL SKETCH .......................................................................................... 102
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LIST OF TABLES
Table page 2-1 Insect sampling dates and times from Mangifera indica over the entire 8-
week blooming period at three orchard sites in Miami-Dade County, Florida. .... 45
2-2 Total number of insects collected throughout the 8-week blooming period ........ 46
2-3 Insects most prevalent throughout the 8-week mango blooming period (Jan. 23 to March 16, 2018) at 3 mango orchards in south Florida. ............................ 47
2-4 The percentage of Diptera collected throughout the 8-week blooming period .... 48
2-5 The percentage of Coleoptera collected throughout the 8-week blooming period ................................................................................................................. 49
2-6 The percentage of Hemiptera collected throughout the 8-week blooming period ................................................................................................................. 50
2-7 The percentage of Hymenoptera collected throughout the 8-week blooming period ................................................................................................................. 51
2-8 The percentage of Thysanoptera collected throughout the 8-week blooming period ................................................................................................................. 52
3-1 Observed insects on ‘Keitt’ mango flowers (Mangifera indica) ........................... 72
3-2 Quantification of mango (Mangifera indica) pollen on insects collected from ‘Keitt’ mango trees .............................................................................................. 73
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LIST OF FIGURES
Figure page 2-1 Orchard 1 (25°30’22.04” N 80°29’56.4 W) on January 1, 2018, during the
beginning of panicle emergence. ........................................................................ 53
2-2 Orchard 2 (25°29’50.15” N 80°29’25.64 W) a commercial orchard on February 13, 2018, during the completion of panicle emergence and flower opening ............................................................................................................... 54
2-3 Orchard 3 (25°35’58.96” N 80°26’43.96 W), commercial orchard on January 25, 2018, during early panicle emergence and flowering which was sparse. ..... 55
2-4 Most abundant insect orders collected from three mango orchards in south Florida during the 2018 8-week blooming period in south Florida ...................... 56
2-5 The five most prevalent Dipteran families collected on Mangifera indica throughout the 8-week blooming period across the three orchards in south Florida. ............................................................................................................... 57
2-6 Comparison of the four most prevalent Chloropidae genera collected from three mango (Mangifera indica) orchards in south Florida during the 2018 8-week blooming period ......................................................................................... 58
2-7 Comparison of the two most prevalent Chloropidae genera collected from three mango (Mangifera indica) orchards in south Florida ................................. 59
3-1 The mean number of flowers visited on ‘Keitt’ mango (Mangifera indica) at the Tropical Research and Education Center, Homestead, Florida .................... 74
3-2 The mean visual observation time insects visited ‘Keitt’ mango (Mangifera indica) inflorescences ......................................................................................... 75
4-1 Pollinator exclusion bags (middle-right side) in the canopy of ‘Keitt’ mango trees ................................................................................................................... 83
4-2 Pollination exclusion bag placed around a mango inflorescence prior to anthesis on January 30, 2018. ............................................................................ 84
4-3 A developing mango inflorescence on March 1, 2018, inside an exclusion bag. .................................................................................................................... 85
4-4 A bagged panicle with no fruit-set or vegetative growth (March 15, 2018). ........ 86
4-5 Initial fruit set on ‘Keitt’ mango. Fruit set varies throughout the panicle (March 1, 2018). ................................................................................................. 87
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4-6 Fruit enlarging after initial fruit set (March 15, 2018). ......................................... 88
4-7 Fully developed fruit on July 28, 2018 at the Tropical Research Center, Homestead, Florida. ........................................................................................... 89
4-8 The mean number (± SE) of fruit per panicle on non-bagged and bagged (insects excluded) mango inflorescences on March 2, 2018 .............................. 91
4-9 The mean number (± SE) of fruit on non-bagged and bagged inflorescences on May 10, 2018, 140 days after bagging. ......................................................... 93
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Abstract of Thesis Presented to the Graduate School of the University of Florida in Partial Fulfillment of the Requirements for the Degree of Master of Science
AGROECOLOGICAL ANALYSIS OF ARTHROPODS INVOLVED IN MANGO
POLLINATION IN SOUTH FLORIDA
By
Matthew Quenaudon
May 2019
Chair: Daniel Carrillo Major: Entomology and Nematology
The role of insects on pollination of Mangifera indica is poorly understood. We
identified the most abundant arthropods visiting mango flowers, their interaction with
mango flowers, and how much mango pollen they are carrying. A total of 4,564 insects
were collected from mango flowers during the entire mango bloom period (8 weeks) in
three mango orchards located in Homestead, Florida. Hippelates sp., Liohippelates sp.,
and Oscinella sp. were the most abundant insects during the peak flowering period
when mango flowers are more receptive to pollination. Drosophilids, Sciarids,
Cryptophagus sp., and Cicadellids were present across the entire mango blooming
period. Cardiastethus sp., Dagbertus sp., Microtechnites sp., Zaprionus sp., and
Frankliniella sp. were abundant during the last two weeks of the mango bloom. Apis
mellifera carried large amounts of pollen but was rare in mango orchards. Muscids,
Allograpta obliqua, and Camponotus planatus were also observed to average high
pollen counts. Camponotus floridanus visited more mango flowers per unit of time,
followed by Calliphorids, Syrphids, and Apis mellifera. An arthropod exclusion test
revealed that insects may increase fruit set up to 17%. Our results indicate that a wide
diversity of insects pollinate mango in Florida and there are temporal shifts in insects
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throughout the mango bloom. Musca domestica, Allograpta oblique, Forcipomyia
genualis, Liohippelates sp., Hippelates sp., Camponotus floridanus, Camponotus
plantatus, and Apis mellifera are the most important insects providing pollination
services in mango in Florida as indicated by their visitation frequency and/or their pollen
loads. Differences in insect populations in separate orchards suggest that cultural
practices may influence insect populations and could be used to augment pollinator
populations.
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CHAPTER 1 LITERATURE REVIEW
Origin, Distribution, and Importance of Mangifera indica
Mango (Mangifera indica) is a major fruit crop of the tropics and subtropics
worldwide. The center of origin of mango is eastern India and southern Asia. There are
two basic types of mango, which are distinguished by mode of reproduction and
generalized fruit characteristics. The Indian mango type is indigenous to the subtropics
and northeastern India and typically possesses a monoembryonic seed while the
southeastern Asian mango is indigenous to tropical Asia and possesses a
polyembryonic seed (Iyer and Schnell, 2009). A monoembryonic seed contains only a
single zygotic embryo, with characteristics of its male and female parents.
Polyembryonic seeds possess multiple embryos, one of which may be zygotic but all
the rest are clones of the female parent. ‘Keitt’ is a monoembryonic-type mango that
requires grafting in order to be perpetuated. Grafting is used to reduce the time it takes
a tree to produce fruit and is a more economical approach (Campbell, et al. 2002).
Through the European voyages of the 15th and 16th centuries, mango spread
globally. Mango transportation had to occur as ripe fruit, seedlings, or grafted plants
because mango seeds could not survive freezing or drying (Mukherjee, 2009). The
Portuguese were responsible for introducing the mango from their Indian colonies to
Africa and later to the Americas (Mukherjee, 2009). Over time the polyembryonic mango
varieties were brought through the Pacific trading ports of Mexico and Panama into the
New World colonies, and from there to the West Indies. The first introduction into
Florida was a polyembryonic seedling brought from Cuba in 1861 (Mukherjee, 2009).
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The diversity of the U.S. mango gene pool continued to increase and by the 20th
century there was mango germplasm from India, Cambodia, the Philippines, and other
areas in southeast Asia (Mukherjee, 2009). Despite the vast amount of mango
germplasm introductions into Florida, it is estimated that most of the Florida cultivars are
descended from four monoembryonic Indian mango cultivars (‘Amini’, ‘Sandersha’,
‘Mulgoba’, and ‘Bombay’) and one polyembryonic cultivar (‘Turpentine’) from the West
Indies (Schnell et al., 1995).
Mango production in the U.S. is restricted to California, Florida, Hawaii, and
Puerto Rico (Marzolo and Lee, 2016). Despite having many influential cultivars, the
U.S. is not a major producer or exporter of mangoes and produces a mere 3,000 metric
tons annually (Evans, 2008). India however, accounted for 38.6% (10.79 million metric
tons) of world production between 2003 and 2005 and is the largest producer. The U.S.
is, however, the top importer of fresh mangoes with 459,936 metric tons in 2017
according to USDA market news (Mango Volume & Price History, 2018).
Florida is the largest producer of mangoes in the U.S. (Draper, 2014). Florida
grows about 150,000 mango trees on approximately 1,350 acres, producing an
estimated 370,000 bushels (~20.4 million pounds) with an estimated value of $5.6
million (Crane, 2018). Production of mango in Florida is limited largely due to climate
requirements. The mango season in Florida extends up to 6 months from early May to
October (Marzolo and Lee, 2016). Flowering is affected by inherent genetics, previous
and current weather conditions, soil moisture, and cultural practices. Panicle emergence
and flowering may begin anytime from late December through April. However, one way
of increasing mango production in existing plantings is to increase fruit set through
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improved pollination. The relationship between pollination and fruit set is important to
understand, as pollination and fertilization are essential yield-limiting constraints, as
evidenced by the high density of flowers compared to fruit set quantities per tree
(Davenport, 2009). Insects play a major role as pollinators of many agricultural crops
including mango (Ramirez and Davenport, 2016). In Florida mangoes, however, the role
of insects in pollination is poorly understood.
Reproductive Physiology and Floral Biology
In order to best understand the role and impact of insects in pollination, it is
essential to understand the floral biology of mango. The sex ratio amongst perfect
(pistil and staminate structures) to staminate flowers (only male structures) varies with
cultivar and climate (weather conditions) and within each panicle (Davenport, 2009).
Physical and environmental conditions can also play a role in this variability, although
the terminals of inflorescences contain more perfect flowers compared to the panicle
axis, where staminate flowers are more clustered (Davenport, 2009). Perfect flowers
seem to make up the final vertical spike of a panicle, however following anthesis, the
flowers closer to the panicle axis fall off and the sex ratio fluctuates (Davenport, 2009).
Mango shoots undergo different phenological stages, beginning with cell division
in the apical and lateral meristems (Ramirez and Davenport, 2010). This cell division
results in stem flushes that are either synchronous or asynchronous throughout the
canopy (Ramirez and Davenport, 2010). Davenport (2007, 2009) stated there are
three main shoot types as a result of cell division. This includes vegetative shoots that
form leaves and stems, generative shoots that form the inflorescence, and mixed shoots
that may possess both leaves and inflorescences within the same node (Davenport,
2007, 2009; Ramirez and Davenport, 2010). The vegetative appearance of leaves
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changes as the leaves mature; initially light green and then turning reddish generally
two weeks after initial bud break (Ramirez and Davenport, 2010). Mango tree
development is tied to genetic predisposition, climate, and other biotic factors.
Vegetative growth flushes generally take place during warmer temperatures, 25°C or
higher, and take roughly three to six weeks for full maturation (Ramirez and Davenport,
2010). This can be exhibited when comparing subtropical to tropical mango
development, where a distinct time gap between vegetative and reproductive stages is
present under subtropical conditions but not tropical conditions under which fruit,
flowers, and vegetation can be intermingled on the same canopy at the same time
(Ramirez and Davenport, 2010).
The sex ratio, i.e. ratio of perfect to male flowers, is determined prior to and
during flowering by both environmental and physiological factors. Cool weather, which
is more common during the early flowering period, may limit perfect flower development
(Davenport, 2009). In contrast, warmer temperatures promote the occurrence of perfect
flowers sometimes reaching a two to seven-fold increase (Majumder and Mukherjee,
1961; Davenport, 2009). Endogenous factors such as hormones and exogenously
applied plant growth regulators may modify the sex ratio of inflorescences (Davenport,
2009). The combination of gibberellic acid (GA3) and urea for instance, when applied
right before inflorescence shoot initiation, will result in a decline of the number of perfect
flowers (Rajput and Singh, 1989; Davenport, 2009). In comparison, the application of
paclobutrazol (an inhibitor of GA3) to the soil and naphthalene acetic acid (NAA) has
been shown to increase the perfect to staminate flower ratios, and foliar applications of
BA (benzylaminopurine) with 2% calcium ion increased the percentage of perfect
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flowers (Singh and Rajput, 1990; Kurian and Iyer, 1993; Mallik et al., 1959; Singh et al.,
1965; Davenport, 2009). Despite the ability to manipulate sex ratios and increase
perfect to staminate flower ratios, there has been no evidence to suggest increased fruit
yield from chemically increased sex ratios, implying perfect flower ratios are not the
limiting factor in crop performance (Schaffer et al., 1994; Davenport, 2009). Davenport
(2009) theorized that pollen viability, inflorescence growth, and ovule fertilization are the
main factors resulting in low fruit set. Thus, an increased understanding of the role of
insects involved in mango pollination and fruit set may greatly improve mango fruit
production.
Insect Pollinators
A deeper understanding of the insects involved in the pollination of mango
cultivars may lead to cultural practices that improve pollination and result in greater fruit
set. Popenoe (1917) and Davenport (2009) first suggested that pollen transfer amongst
mango flowers was accomplished primarily by insects as opposed to earlier ideas that
mangoes were primarily wind pollinated. Early observations suggested the most
efficient pollinators listed in order of importance included wasps, bees, large ants, and
large flies (Anderson et al., 1982; Davenport, 2009). Depending on various abiotic
factors such as wind, rain, and temperature, differences in insect pollination rates may
occur. Young (1942) observed that insects visited only 10-12% of mango flowers
predominantly in the morning and evening, with some visitation at night. In general,
knowledge about the role of insects in cross-pollination is limited (Anderson et al.,
1982), as key species were not identified and no observations were made of pollen
transfer and pollen deposition by insects in previous studies (Anderson et al., 1982;
Davenport, 2009).
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Ne’eman et al. (2010) postulated that one of the main proxies for evaluating a
pollinator’s impact on fruit set is to look at pollination efficiency, which depends on the
‘frequency’ of flower visitation and ‘effectiveness’ of pollen deposition. Pollination
deposition effectiveness can be estimated by the sheer number of pollen grains
deposited on the stigmas. However, pollen deposition effectiveness also depends on
how likely the pollen deposition will result in seed set per flower, which is influenced by
stigma receptivity and pollen quality. If a stigma is not receptive, it will be unable to
recognize the pollen, and/or the pollen will not adhere to the stigmatic surface. If pollen
has been tainted or degraded, the viable pollen to ovule ratio may be decreased,
resulting in a reduction in seed set (Ne’eman et al., 2010).
Pollen deposition effectiveness is also tied to the insect’s morphology and pollen
carrying capacity. With this understanding, most bees, given their distinct
morphological trait of having a corbicula or scopa to allow for carrying relatively large
amounts of pollen, would be high on the pollen deposition effectiveness scale.
However, just because an insect does not have the capability to transfer large amounts
of pollen does not mean it is not a good pollinator, as some insects may have a much
higher population density or higher preference for a plant, leading to an increase in
flower visitation frequency. Ne’eman et al. (2010) foresaw this issue, taking into
consideration that continuous visitation from a pollinator to a plant species may
contribute to effective pollination even when per-visit pollen deposition is low. However,
King et al. (2013) postulated that frequency of visitation is a poor representation for
overall pollination effectiveness (PE) and proposed the single visit deposition (SVD)
method to distinguish ‘true’ pollinators from insects just visiting flowers.
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The SVD method focuses on quantifying pollen deposition on virgin stigmas
during a single visit by a given insect, achieved through bagging flowers and excluding
other visitors. Nevertheless, King et al. (2013) recognized the potential limitation of the
SVD method to evaluate the importance of different pollinators, namely that the method
may result in unnatural flower visitor identity or behavior due to delayed removal of bags
on the flowers. Moreover, King et al. (2013) suggested that the SVD method provide
better PE assessments for those insects that are similar in size to the flower, feed
rapidly, and gather pollen on their body quickly. Using the SVD method to identify PE
may be even more skewed in a single inflorescence versus panicle inflorescences,
given that there may be a minimum threshold of pollen grains required in order for fruit
set to occur. The determinant inflorescence on mangoes, or cymes, contain an apex
bud which is the primary bloom followed by lateral buds which may lead to another set
of cymes and delayed bloom. This process is heavily dependent on both biotic and
abiotic factors, and thousands of blooms generally span over several months, allowing
for a much longer timeframe in which insects and other pollinators may contribute to
pollination. An overall high abundance of insects depositing less pollen per visit could
surpass the total amount of pollen deposited by larger but less frequently visiting insects
such as bees. For this reason, it is crucial to observe and understand the unmanaged
insect fauna that may be contributing to pollination.
The collective role of unmanaged insects can be just as important and useful for
the pollination of crops as compared to managed pollinators. Rader et al. (2012) looked
at the importance of unmanaged insects including bees on crop pollination and found
varying degrees of evidence for the importance of unmanaged insects. Insects visiting
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Brassica rapa flowers in four different fields were observed over the course of 4 years.
After 42,032 visits, the most prevalent visitors included Apis melifera (honey bee) and
seven unmanaged insect species. While honeybees were responsible for 40-60% of all
visits compared to 39.2% of the unmanaged insects, in two out of the four years
unmanaged insects were able to deliver more efficient and consistent pollination
services compared to the honeybee.
Decreases in bee populations due to limited gene pools, insecticides, and the
presence of disease and parasites (Bartomeus et al., 2013), reinforce the importance of
a better understanding of the other insects involved in mango pollination. As
landscapes and crops change, some populations of insects will falter while others will
rise, making it important to understand whether insects that can thrive in human-altered
ecosystems will deliver the pollination services previously provided by other insects.
These developments have motivated studies examining looking at the local fauna of a
given location to see what is really pollinating crops, including both managed and
unmanaged pollinators.
Sung et al. (2006) looked at pollinators of mango flowers in southern Taiwan.
The most common insects collected during 60 min intervals between 9 am and 1 pm
included bees, Apis cerana, A. mellifera, Braunsapis hewitti, Halictus sp., and flies,
Chrysomya megacephala, Musca domestica, Menochilus sexmaculatus, and
Indioscopus sp. (Sung et al., 2006). Of all the insects collected, 69.1% were female and
42.0% were flies (Diptera). The most dominant insect pollinators included Apis sp.,
Halictus sp., and C. megacephala. Diptera were considered unmanaged insects that
often congregated in larger densities than Hymenoptera while the bee species A. cerna
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and A. mellifera were considered managed. Small arthropods such as mites, thrips,
small flies, and parasitoids were all disregarded and not accounted for, and thus their
sample size contained only 126 insects observed at nine different locations over a 32-
day period (Sung et al., 2006). However, there was insufficient data to conclude which
insects were most responsible for pollination and fruit set.
Huda et al. (2015) determined that large flies, such as Eristalinus sp. and
Chrysomya sp. in the Syrphidae and Calliphoridae families respectively, were pollen
carriers and efficient pollinators of mangoes in Malaysia. Insect morphological traits
and size effects in pollination and pollen carrying capacity were investigated. The most
important Dipteran was an Eristalinus sp., possessing the greatest number of pollen
grains on its body with a Stomorhina sp. and Chrysomya sp. following. However, the
Eristalinus sp. was rarely found in mango orchards. Both Sarcophaga sp. and
Camponotus sp., a large fly and ant, contained very few pollen grains on their bodies
(Huda et al., 2015). A smaller ant, Iridomyrmex sp., did not carry any pollen, possibly
because of its often-observed grooming habits. When comparing males to females,
anthophilous females often had less pollen on their bodies than males (Huda et al.,
2015). This could be attributed to differences in head size between sexes, considering
no differences in body length between sexes were found (Huda et al., 2015).
Interestingly, insects with a large head width, as opposed to head length, had greater
pollen reserves on them, and overall larger pollinators contained more pollen (Huda et
al., 2015). This relationship holds true for several insect genera, but varies amongst the
Diptera, where size of the insect seemed to vary with the pollen capacity of an individual
insect (Huda et al., 2015). Augmentation of Eristalinus spp., Chrysomya spp.,
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Stomohina spp., Sarcophaga spp., and Camponotus spp. is believed to improve
pollination, as these insects have relatively large body parts and hairy bodies (Huda et
al., 2015).
Pollinator effectiveness may be higher for those insects that occur in high
densities in an area and actively forage amongst flowers with high visitations rates,
allowing them to encounter the stigma and pollen grains (Rader et al., 2009). In
addition to insect morphology, the behavior of an insect can influence its ability to be an
efficient pollinator (Huda et al., 2015). Insects that have high visitation rates but spend
less time per flower may allow for a greater spread of pollen throughout the field,
however, the amount of pollen delivered per visit may vary. This can be compared to
insects that have a lower visitation frequency, but a longer duration of interaction on the
flower and stigma, possibly resulting in more pollen deposition per visit. Additionally,
insects show different methods of foraging for nectar and may side-work (behavior in
which an insect approaches) a flower resulting in less stigmatic contact leading to
reduced seed set per visit (Park et al., 2016). This suggests that understanding the
individual insect’s behavior is just as important as evaluating the density and frequency
of an insect in an orchard.
Research has helped further shape an understanding of the importance of
insects and the impact that they have in the pollination of mangoes. Previous reports
indicated the presence and importance of Hymenoptera, Diptera, and other insects in
mango production. Although certain insects such as Syrphidae, Apis sp., and
Calliphoridae, make an appearance across different mango production regions, some of
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the more recent studies reveal the significance of understanding the insect fauna at an
orchard level as insect communities can vary across regions.
Objectives of Master of Science Thesis Research
1. Determine and identify the most frequent arthropod visitors on ‘Keitt’ mango
flowers at three separate orchards over the entire mango blooming period.
2. Determine the behavior of the most common arthropods during flower
visitation; duration and interaction with flowers and flower structures and the amount of
pollen they are transporting.
3. Determine the importance of arthropods in pollination and crop production
through comparison of fruit set within bagged and non-bagged inflorescences.
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CHAPTER 2 MOST FREQUENT ARTHROPOD VISITORS ON ‘KEITT’ MANGO (MANGIFERA
INDICA) FLOWERS IN SOUTH FLORIDA
Introduction
Mango (Mangifera indica) is one of the world’s major fruit crops in the tropics and
subtropics. The monoembryonic and polyembryonic seed are the two main types of
mangoes, with the latter pertaining to tropical Asia and the former being significant to
India (Litz, 2009). ‘Keitt’ mango is a monoembryonic-type mango cultivar and is
especially important to Florida, being a dual-purpose fruit and a major commercial
variety (Crane, 2018). Dual-purpose signifies the ability of the fruit to be eaten either as
a green fruit that is popular amongst Asian-Americans or as a ripe fruit. Production in
Florida is less about volume but rather more focused on producing a diverse array of
mango cultivars and specialty types (e.g., green market, fresh market, specialty food
service market). Puerto Rico and Florida are the largest producers of mangoes in the
U.S. (Draper, 2014).
Despite producing an estimated value of $5.6 million annually in Florida (Crane,
2018), two of the main limiting factors to production are weather (i.e., potential freeze
events) and land availability. One way to increase mango production is through
improved pollination to increase fruit set. Florida growers have attempted using honey
bees to increase pollination, however, mango flowers do not appear to be overly
attractive to honey bees (Popenoe, 1917). Around the world different insects including
Musca domestica, Chrysomya megacephala, Cantharis sp., Apis cera, and Apis
mellifera have been found to be important pollinators of mangoes (Sung et al., 2006). In
Florida mangoes, the insects responsible for pollination are poorly understood and this
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lack of understanding limits the development of cultivation strategies to improve
pollination.
Further insights into the insects pollinating mango cultivars in the south Florida
region could result in changes to cultural practices that improve pollination and increase
fruit set. The population of the well-known and studied honey bee, Apis melifera, has
been in decline worldwide due to Colony Collapse Disorder, the Varroa destructor
parasitic mite, loss of habitat, in-breeding, and insecticides (Rader et al., 2009). It is
therefore imperative to look to other, unknown and unmanaged insects for “pollination
insurance” (Winfree et al., 2007). These are insects that can pollinate the intended
target in the absence of the managed pollinators such as honey bees. While studies
have focused on the dieback of honeybees and the subsequent native bees that may
become more significant in the pollination of crops, much of this focus has been on
different unmanaged hymenopteran pollinators.
While hymenoptera, especially Apidae, are known for their strong pollination
capabilities, non-hymenopteran insects such as Stratiomyidae and Syrphidae (Diptera)
have been shown to carry pollen up to 400 m, 100 m more than bees including
Halictidae and Apidae (Rader et al., 2011). The species richness of crop pollinators
may often be overlooked, though numerous studies have found that a diversity of
unmanaged pollinators results in greater pollination and crop yields (Klein et al., 2007).
Although some crops may see better fruit set with particular bees, and some bees may
prefer select crops, there is a tremendous number of insects being overlooked for their
pollination contribution.
25
The use of unmanaged insects supports the idea that numerous insect species
with high visitation frequency are capable of providing the “pollination insurance”
previously discussed. Winfree (2007) determined through both empirical and simulation
results that native bees were the most important and alone were capable of adequately
pollinating watermelon crops. Manipulating an insect’s population by maintaining
natural sites and implementing sustainable cultural practices (e.g., not mowing row-
middles all year and not applying pesticides within a window before and during the
flowering period) may increase pollinator frequency and improve pollination rates. Prior
to manipulating an environment to better favor specific insects, it is vital to understand
which insects are present in the agroecosystem and visiting the crop flowers.
In this study we hypothesize that numerous Hymenoptera and Diptera insects
are the main pollinators for mangoes in the south Florida region. The objectives of this
investigation were to: (1) determine the most frequent arthropod visitors on ‘Keitt’
mango flowers, (2) examine variation in insect visitation across three separate orchards
over the entire mango blooming period, and (3) determine how arthropod visitation rates
differed depending on the time of day.
Material and Methods
To gain a better understanding of the diversity of species contributing to the
pollination of mango flowers, three ‘Keitt’ mango orchards were identified and sampled
over the entire 2018 mango blooming period (eight weeks). Orchard 1 (25°30’22.04” N
80°29’56.4 W) was located at the Tropical Research and Education Center (TREC)
(Figure 2-1). TREC maintains a regular weed control (i.e., mowing and herbicide
applications) and fertilizer program (granular NPK-Mg, foliar minor element applications,
and soil-drench chelated-Fe) throughout the year. The disease control program includes
26
fungicide-spraying from flowering to harvest as needed. The application of the fungicide
Bravo Weather Stik (chlorothalonil) occured January 2, 10, and 22, 2018 and the
herbicide Roundup Max (glyphosate) was made on January 11, 2018. Between
February 5 and June 4, 2018, the fungicide Penncozeb 75 DF (mancozeb) with the
adjuvant Nu Film 17 (pinene sticker) was sprayed intermittently eight different times.
Another fungicide, Satori (azoxystrobin) was sprayed on April 30 and May 9, 2018. The
off-season cultural program is comprised mostly of weed control and one application of
the insecticide, malathion on December 19, 2017. All products were applied at
recommended label rates. Orchard 2 (25°29’50.15” N 80°29’25.64 W) is a commercial
orchard located within 2 miles of TREC, where similar maintenance is undertaken but it
contains more weeds and wild flowers in the understory (Figure 2-2). Boron and Bravo
(chlorothalonil) were sprayed multiple times through the 8-week blooming period.
Penncozeb 75 DF (mancozeb) with Mn, ZnNO3, MgSO4 were applied on February 26,
2018. Penncozeb was sprayed again on March 6, 13, and 20, 2018. On March 20, a
fungicide and bactericide Kphite 7LP (mono and dipotassium salts of phosophorous
acid) was sprayed. The fungicide Switch (cyprodinil and fludioxonil) was applied on
March 30, 2018. Orchard 3 (25°35’58.96” N 80°26’43.96 W) was located roughly 10
miles from TREC, where a wide variety of fungicides and herbicides were applied
(Figure 2-3). Manzate Pro-Stick (mancozeb), Nu Film 17 (pinene polymer sticker),
Urea, Micorthiol Disperss (sulfur), Gramoxone SL 2.0 (paraquat), Liberty 280SL
(glufosinate ammonium), Freeway (organosilicone surfactant), Level 7 (nonionic
surfactant, spreader), and Cuprofix Ultra 40 (copper) were all applied throughout the
27
blooming period. This orchard had interconnecting canopies so the area beneath the
canopy received very little sunlight.
Each orchard was sampled once per week but differed in the sampling frequency
per day. Orchard 1 was sampled 3 times in a day (8-10 am, 1-3 pm, and 8-10 pm) and
Orchards 2 and 3 were sampled two times in a day (8-10 am and 1-3 pm) (Table 2-1).
Ten ‘Keitt’ mango trees were selected randomly throughout each orchard and five
randomly selected inflorescences within seven feet of the soil surface per tree were
used for sweep net collection. As there were insufficient trees with inflorescences
during the first week, blooming trees were initially selected. Inflorescences were swept
in a single motion using an insect sweep net, where the entire bag quickly engulfed the
branch of the inflorescence. Once completely covered, the sweep net was pulled to the
side and twisted, as to not allow any arthropods to escape. Prior to sweeping the next
inflorescence, the sweep net was briefly shaken, untwisted, and then swept over the
next inflorescence. Once five randomly selected inflorescences per tree had been
swept, the contents in the sweep net were immediately placed into a plastic bag that
was stored in a freezer (0C) for further identification. On the same trees, an additional
sample was collected using a beat cloth to capture smaller arthropods not collected
from the sweep net or missed due to small size and/or clinging to the flowers. A white
collection tray measuring 32 x 45 cm was lined with paper towel and misted with water
to help keep the insects docile. Each inflorescence was lightly shaken over the
collection tray to catch falling insects. Two of the five inflorescences used for the sweep
netting were chosen at random and this comprised a single beat cloth sample.
28
The time of collection at each site can be viewed in Table 2-1. Orchard 1 was
the only site sampled at night due to logistical reasons and availability. Due to weather
and lack of insects collected, nighttime collections (7-9 pm) took place for 7 of the 8
weeks. Over the course of the 8-week blooming period, inflorescence accessibility
changed from the first to the last samples collected. During weeks 1 through 4 there
was an increase in new blooms while a healthy bloom population was maintained during
weeks 5 and 6. During weeks 7 and 8 healthy blooms decreased and limited flowers
were available for pollination. Once a collection was completed at each location,
specimens were brought back to the lab for identification and study. Some samples
were sent to a state taxonomist, Dr. Gary Steck, Florida Department of Agriculture and
Consumer Services, for identification. The data collected includes:
Number of organisms collected
Number of different species (species richness)
Species evenness (how close in numbers are the species)
Location of collection (orchard)
Results
The total number of insects collected from inflorescences in three ‘Keitt’ mango
orchards using both sweep net and beat cloth methods over the 8-week blooming
period was 4,564. A total of 14 orders and 78 families were identified (Figure 2-4).
Thysanoptera was the most abundant order with a total of 1,663 insects which
comprised 36% of all insects collected. However, almost all thrips (1,160 of the 1,663)
were collected in week 8 of the collection. Diptera was the second most abundant order
with 1,293 insects (28% of total insects collected) and was distributed across all three
orchards with 885 from Orchard 1, 201 from Orchard 2, and 207 from Orchard 3. The
next most abundant order was Hemiptera with 766 insects at 17% of the total collected.
29
There were 406 (9%) coleopterans, 184 (4%) hymenopterans, and 137 (3%) arachnids.
The remaining orders were Neuroptera at 54 insects, Lepidoptera at 48, Pscoptera at 6,
Trichoptera at 3, Orthoptera at 2, Odonata at 1, and Collembola at 1.
The total number of insects collected differed among the three orchards (Table 2-
2). Orchard 2 was the most abundant with 2,377 total insects followed by Orchard 1
with 1,811 insects and Orchard 3 with 376 insects. Distribution of the most abundant
orders was even across the orchards with the exception of Thysanoptera, which was
more abundant in Orchard 2 with 1,471 thrips compared to Orchard 3 with only 32
thrips. Insects from nine orders were collected in all orchards but only Orchard 1
included insects from the Collembola, Odonata, Orthoptera, and Trichoptera orders
Order Diptera
The top 5 most prevalent families of dipterans collected throughout the 8-week
mango blooming period included Chloropidae, Drosophilidae, Sciaridae,
Ceratopogonidae, and Muscidae (Figure 2-5). The chloropids comprised 54% of the
total, with 698 insects followed by Drosophilidae, Sciaridae, and Ceratopogonidae with
approximately133-169 insects each. Muscidae had the fewest insects but were present
in all three mango orchards (Table 2-3). Muscids were collected all weeks except for
week 7 and were mainly collected in Orchards 1 and 2 (n = 10 and 9, respectively)
(Table 2-3). Chloropidae were the most abundant during the first 3 weeks, declining
from week 3 through week 8. Drosophilidae were consistently present across all 8
weeks, with 96 out of the 169 collected in Orchard 3. Sciaridae peaked in week 4 with
82 insects before decreasing in weeks 5 through 8 to population numbers similar to
weeks 1 through 3. Ceratopogonidae were predominantly found in Orchard 1, with 98
out of 137, and well represented across all 8 weeks.
30
Chloropidae
The Chloropids collected consisted of 4 genera: 246 Hippelates sp., 301
Liohippelates sp., 121 Oscinella sp., 15 Ceratobarys sp., and 15 unidentified species;
representing 54% of all Diptera collected. The two most prevalent Chloropids,
Hippelates sp. and Liohippelates sp., were very similar in size, shape, and color and
could be mistaken for each other at first observation. Three out of the 4 genera of
Chloropidae were collected predominantly in the morning sampling, with fewer in the
afternoon and nightly collections even lower (Figure 2-6). Unlike the other genera, the
number of Oscinella sp. collected was similar throughout the three orchards and the
time of day.
The chloropids were highly abundant and well represented in all three orchards.
Both Hippelates sp. and Liohippelates sp. were captured at each location in relatively
equal numbers (Figure 2-7). These two genera represent a large number of individual
species that are both abundant and appear to be well distributed in mango orchards of
south Florida.
Drosophilidae
The second most abundant dipteran family, Drosophilidae, consisted of four
species, Drosophila sp., Zaprionus indianus, Scaptomyza sp., and an unidentified
species (Table 2-4). These four species were captured primarily during the morning.
Drosophila sp. was found in all three orchards 7 out of the 8 weeks, Z. indianus in two
orchards 3 out of the 8 weeks, and the unidentified species in all three orchards 7 out of
the 8 sampled weeks. However, 27 out of the 28 Z. indianus were collected in Orchard
3 on a single inflorescence.
31
Sciaridae
Two species of Sciaridae, Odontosciara sp. and an unidentified fungus gnat,
were found visiting mango flowers mostly at night and primarily from one grove with 121
out of a total of 133 collected at Orchard 1. The remaining 12 sciarids were collected at
Orchard 2; none were collected at Orchard 3. Week 4 had the highest populations with
81 specimens collected at Orchard 1, a time when the majority of Diptera and overall
insect populations were lower (Table 2-4).
Muscidae
Atherigona reversura, Musca domestica, and an unidentified species were the
three Muscidae collected visiting mango flowers. Atherigona reversura captures were
split between morning and night in Orchard 1 and 2 whereas other muscids were
collected throughout the day in all three orchards (Table 2-4). Orchard 1 contained 10
muscids, with 9 in Orchard 2 and 2 in Orchard 3.
Syrphidae
An assortment of syrphid flies including Ornidia obesa, Allograpta obliqua,
Toxomerus watsoni, Toxomerus marginatus, Copestylum violaceum, and Palpada
alhambra were collected primarily in the morning and afternoon (Table 2-4). Orchard 1
contained the most syrphids with 8 total, followed by Orchard 2 with 3 and Orchard 3
with 2.
Calliphoridae
The blowfly Lucilia coeruleiviridis was collected in two orchards (Table 2-4). The
4 calliphorids collected were split between Orchard 2 and 3 and were collected in weeks
1, 4, and 6.
32
Ceratopogonidae
Four species of Ceratopogonidae were found during the day and night in all three
orchards and throughout the entire 8-week blooming period; Forcipomyia genualis,
Forcipomyia biannulate, Forcipomyia spp and Artichopogon warmkei (Table 2-4). Most
ceratopogonids (106 of 154) were collected from Orchard 1.
Order Coleoptera
A total of 406 beetles were collected, comprising 9% of the total insects collected
(Figure 2-4). The majority of these (346) were collected in Orchard 1, generally
scattered throughout the sample weeks. Cryptophagus sp. were the most abundant
with a total of 330 insects (Table 2-3). Species collected include Cryptophagus sp.,
Diabrotica balteata, Diaprepres abbreviatus, Delphastus sp., Myllocerus
undecimpustulatus, Haromia axyridis, Euphoria sepulcralis, Melanophthalma sp.,
Hypothenemus sp., Brachiacantha barberi, Scymnus cervicalis, Cryptocephalus
irroratus, Cycloneda sanguinea, Diomus sp., and Diachus auratus (Table 2-5).
Cryptophagidae
A total of 330 Cryptophagus sp. were collected, during the morning, afternoon,
and night sampling (29.1, 33.9, and 37.0% of all samples, respectively) (Table 2-3).
Although 302 out of the 330 Cryptophagus sp. were collected in Orchard 1, the other
two orchards had approximately the same number collected (n = 13 and 15 specimens,
respectively). Cryptophagidae numbers gradually increased until weeks 6 and 7, when
populations were 101 and 99 specimens collected, respectively.
Coccinellidae
Seven coccinellid species were collected which included B. barberi, C.
sanguinea, Delphastus sp., Diomus sp., Harmonia axyridis, and Scymnus cervicalis and
33
an unidentified species. These insects were found in relatively low abundance, only
comprising a total of 22 specimens (Table 2-5). Thirteen coccinellids were found in
Orchard 1, 7 in Orchard 2 and 2 in Orchard 3. All Coccinellidae were found in the
morning and afternoon sampling and were mostly collected starting in week 4 and
through week 8.
Curculionidae
Five curculionid species were collected including D. abbreviatus, Hypothenemus
sp., Myllocerus undecimpustulatus, Scolytinae sp., and one unidentified species (Table
2-5). The majority of these insects were rarely found and were mostly comprised of M.
undecimpustulatus (n = 18 out of the 28 curculionids collected). All 18 M.
undecimpustulatus were found in orchard 3 and were caught between weeks 2 and 6.
The damage caused by this curculionid was highly noticeable in orchard 3 and it was
evident the pest was well established in this location. Feeding damage on the mango
foliage was obvious with leaf notching and feeding alongside leaf veins.
Order Hemiptera
Thirteen different families with 23 species of Hemiptera were collected over the
8-week blooming period (Table 2-6). Families include Anthocoridae, Aphididae,
Cercopidae, Cicadellidae, Delphacidae, Flatidae, Geocoridae, Lygaidae, Miridae,
Pentatomidae, Psyllidae, Reduviidae, and Rhyparochromidae. Hemiptera represented
16.8% of all insects with 766 collected (Figure 2-4). Most hemipterans were collected
during weeks 7 and 8 with a total of 476 specimens (62% of the total) collected during
those weeks.
34
Miridae
The mirids represented 59.5% of all Hemiptera and 10% of all insects collected.
Six species of Miridae were present throughout the 8 weeks (Table 2-6). Miridae
collected included Camplyomma verbasci, Dagbertus sp., Lygocoris sp., Microtechnites
bractatus, Pcynoderes atratus and an unidentified species. Dagbertus sp., were
especially abundant during the last two weeks, (n = 293 out of 304 total specimens),
and were found primarily in Orchard 2. Interestingly, Dagbertus sp. were the most
prevalent Hemiptera collected and peaked in abundance during late bloom and fruit set
(weeks 7 and 8) (Table 2-6). Their feeding has been documented to cause flower and
fruit abscission. Initial numbers of Miridae across all three orchards were between 7
and 17 insects per week, which quickly increased to 168 and 222 insects per week for
weeks 7 and 8, respectively.
Cicadellidae
The Cicadellidae were the second most abundant hemipteran family, with a total
of 157 insects (Table 2-6). Two different species were present, Protalebrella
brasiliensis and an unidentified species. The majority of these insects came from
Orchard 1 (n = 107), followed by Orchard 2 (n = 47), and Orchard 3 (n = 10). Unlike the
mirids whose population drastically increased in the last 2 weeks, the cicadellids were
evenly present throughout the 8 weeks. The cicadellid collections increased as the day
progressed with 39 collected in the morning, 55 in the afternoon, and 63 at night (Table
2-6).
Aphididae
Aphids were not well represented and only accounted for 57 total insects and
were predominantly collected in the morning; 32 collected in the morning, 14 in the
35
afternoon, and 10 at night (Table 2-6). Uroleucon sp., Tetraneura sp., and an
unidentified species comprised the aphids collected. Twenty-four aphids were collected
in Orchard 1, 10 in Orchard 2, and 23 in Orchard 3. Aphid populations were most
abundant during the first 3 weeks and increased again in weeks 6 and 7, with lower
abundances in mid-bloom.
Anthocoridae
Four species of Anthocoridae were collected; Amphiareus sp., Cardiastethus sp.,
Orius sp., and an unidentified species (Table 2-6). Cardiastethus sp. were the most
abundant, representing 32 out of the 50 anthocorids, with 25 of these 32 specimens
collected during week 7. Forty-eight of the 50 anthocorids were collected during the
morning and afternoon sampling. Forty-two of the 50 anthocorids collected in Orchard 2
were associated with a high abundance of Frankliniella sp. (Table 2-6).
Other Hemiptera
Individuals from other hemipteran families, including Cercopidae, Delphacidae,
Flatidae, Geocoridae, Lygaeidae, Pentatomidae, Psyllidae, Reduviidae, and
Rhyparochromidae, were less frequent and collectively only represent 5% of Hemiptera
collected.
Order Hymenoptera
The Hymenoptera, a typically important order for pollinators, only accounted for
184 insects; or 4% of all insects collected (Figure 2-4). Families collected include
Apidae, Braconidae, Chalcidoidea, Enyrtidae, Eulophidae, Figitidae, Formicidae,
Halictidae, Ichneumonidae, and Pteromalidae. The most prevalent of these species
were Pheidole sp., Brachymyrmex sp., Quadrastichus sp., Apis mellifera, an
unidentified braconid species, and an unidentified eulophid species. Hymenoptera were
36
evenly represented throughout the 8 weeks, with the highest total in week 7 (n = 43
specimens) (Table 2-7). Most of hymenopterans (166 of 184) were collected in the
morning or afternoon. In addition, 107 of the 184 were collected in Orchard 2, with 47
collected in Orchard 1 and 30 in Orchard 3.
Apidae
Twelve Apis mellifera were collected between weeks 1 and 5, with 8 collected in
Orchard 3, 3 in Orchard 2, and 1 in Orchard 1 (Table 2-7). Most of these insects were
collected in the morning. Honeybees were seldom seen across all three orchards
(personal observations).
Formicidae
The formicids were the most numerous family, encompassing 35% of the total
Hymenoptera with 65 insects collected (Table 2-7). Species include Brachymyrmex sp.,
Camponotus floridanus, Camponotus planatus, Technomyrmex difficilis, Pheidole sp.,
and Tapinoma melanocephalum (Table 2-7). Twenty-five of these insects were
Pheidole sp., all collected from Orchard 2. More formicids were collected from Orchard
2 (n = 46) than Orchards 1 (10 insects) and 3 (9 insects). Most of the formicids were
collected in the morning and afternoon.
Eulophidae
Two species of eulophids were collected; Quadrastichus sp., and an unidentified
species (Table 2-7). There was a total of 45 eulophids, with 37 collected in Orchard 2, 7
in Orchard 1, and 1 in Orchard 3. Most of the eulophids (91%) were collected in the
morning and afternoon. Although no eulophids were collected in week 1, the remaining
weeks had a similar number of specimens collected.
37
Other Hymenoptera
The remaining families of Braconidae, Chalcidoidea, Encyrtidae, Figitidae,
Halictidae, Ichneumonidae, and Pteromalidae and an unidentified species combined
represented 38.5% of all Hymenoptera (Table 2-7). Halictidae, another family known to
be an excellent pollinator, was only found once in Orchard 3. Of all Hymenoptera
collected, all insect families were more numerous in the morning and afternoon, except
for Braconidae, which was collected throughout the morning, afternoon, and night.
Order Lepidoptera
Adults of nine Lepidoptera families collected from mango inflorescences include
Crambidae, Gelechiidae, Geometridae, Gracillariidae, Hesperiidae, Noctuidae,
Tineidae, Tortricidae, and an unidentified species. Forty-eight lepidoptera were
collected, evenly spread out throughout the day with 18 in the morning, 16 in the
afternoon, and 14 at night. Orchard 1 had 18, Orchard 2 had 21, and Orchard 3 had 9.
Populations of Lepidoptera remained low from weeks 1 through 5, then gradually
increased during the last 3 weeks. An unidentified species of Geometridae was the
most numerous with a total of 16 insects. Six were collected in the morning, 9 in the
afternoon, and only 1 at night. Twelve of the 16 geometrids were collected in Orchard
2, with 2 from both Orchard 1 and Orchard 3.
Order Thysanoptera
Four families comprising 7 species were collected, Franklinothrips sp.,
Franklinothrips vespiformis, Frankliniella sp., Frankliniella occidentalis, Frankliniella
fusca, a species of Phlaeothripidae, and an unidentified species were collected
throughout the 8 weeks (Table 2-8). Thysanoptera were the most abundant near the
end of the blooming season with a total of 1,663 specimens; 70.4% of collected thrips
38
were found in week 8 and 1,462 were collected from Orchard 2 alone during weeks 7
and 8. It is important to note that Hemiptera and Thysanoptera populations were
comprised mostly of pests, which increased in the last 3 weeks of collecting when
flowers were no longer receptive and began showing signs of deformity and injury.
Order Araneae
Five different families of spiders were collected during the 8 weeks, with the
majority being several unidentified minute spiders accounting for 128 out of the 137
collected specimens. Araneidae, Linyphiidae, Salticidae, Thomisidae, and the
unidentified small spiders were found predominantly in the afternoon with 62
specimens, followed by morning with 47, and night with 28 specimens. Most spiders
were collected at orchard 1 (90 specimens) followed by orchard 2 (33 specimens) and
orchard 3 (14 specimens).
Insect Dependency on Bloom Period
The most abundant insects collected during the first 3 weeks of bloom, when
pollination is critical, include Hippelates sp., Liohippelates sp., Oscinella sp.,
Drosophilidae, and Apis mellifera (Table 2-3). Those insects most abundant throughout
the entire bloom period include Ceratopogonidae, Drosophila, Sciaridae, Cicadellidae,
Braconidae, and Cryptophagus sp. Insects collected predominantly at the end of the
bloom season during weeks 6 through 8 include Zaprionus sp., Atherigona sp.,
Frankliniella sp., Cardiastethus sp., Campylomma sp., Dagbertus sp., Microtechnites
sp., and Eulophidae sp. Apidae and Syrphidae, two families often associated with
pollination, were seldom caught across the entire bloom period (Table 2-3).
39
Discussion
Pollinator Candidates Based on Population Density
Our findings are similar to those reported previously from India, Malaysia, and
Taiwan (Singh, 1989; Huda et al., 2015; Sung et al., 2006 and Kumar et al., 2012).
Diptera accounted for 28% of the insects collected from the three orchards, including
Syrphidae, Sarcophagidae, Calliphoridae, and Muscidae. Kumar et al. (2016)
concluded that Diptera are neglected pollinators, but studies are continually showing
their importance in pollination. Flies are responsible for pollinating more than 550
different plant species (Kumar et al., 2016), and both Kumar et al. (2016) and Singh
(1989) found that Syrphidae is the most prominent family found visiting mangoes in
India. In addition, Huda (2015) reported Eristalinus spp. (Sirphidae) and Chrysomya
spp. (Calliphoridae) as the most prevalent and important pollinators of mango in
Taiwan. In our study, neither Syrphidae nor Calliphoridae were frequently caught. Out
of 1,293 Diptera caught, only 13 were Syrphidae and 4 were Calliphoridae. However,
these insects move quickly and are difficult to catch with an insect sweep net, which
captures more crawling insects, and may be an underrepresentation of the actual
abundance of these flies in the field.
In contrast, relatively large numbers of Chloropidae, Drosophilidae,
Ceratopogonidae, and Sciaridae were collected. Ceratopogonidae have never been
reported in previous mango studies as most of those studies simply focused on the
large, hairy-bodied flies known to be good pollinators. A species collected during our
sampling, Atrichopogon warmkei, has been stated as a pollinator of Hevea brasiliensis
(Wilkening et al., 1985). Another biting midge in our sampling, Forcipomyia genualis, is
listed as a potential pollinator of mangoes that feeds on flower nectar (Borkent and
40
Spinelli, 2000). Although these insects are small, their sheer population densities and
widespread abundance begs the question as to how important these insects are for
pollination, especially on mango. Chloropidae, Ceratopogonidae, and Drosophilidae
were all found in each of the 3 mango orchards sampled, providing a pattern of
importance. The Chloropidae, Ceratopogonidae, and Sciaridae could often be
observed sitting on an individual flower for several minutes, moving around feeding on
the nectar and pollen. Despite taking longer to visit several flowers, unlike the
Syrphidae and Muscidae that move faster, these small flies displayed a long duration of
interaction with the stigma and stamens that could result in effective pollination.
Three of the most prevalent Chloropidae genera collected were Hippelates sp.,
Liohippelates sp., and Oscinella sp. These insect species have not been reported in
any previous mango pollination study, and thus our results may offer new insights into
the differences in mango pollinators across environments and localities. Liohippelates
sp. are often regarded as an animal pest, given their ability to mechanically transmit
disease in both livestock and humans (Machtinger and Kaufman, 2011). Although
regarded as a nuisance and pest, perhaps new understandings of these irritating flies
could show them to be an important pollinator of mangoes. Large numbers of
Hippelates sp. Liohippelates, and Oscinella sp., were collected in the first 3 weeks of
the mango bloom, a time regarded as a crucial pollination period given the freshness
and receptivity of mango flowers during this time. In total these 3 genera represent
51.7% of all Diptera caught. These insects were caught almost exclusively during the
day, with higher representations during the morning collection (8-10 am) than afternoon
(2-4 pm) collection period. This could be due to greater flower aroma (freshness) during
41
that time of day, i.e. prior to drying of the stigmatic surfaces. Furthermore, morning is
regarded as a crucial pollination period given the higher pollen viability and receptivity of
mango inflorescences (Davenport, 2009). Our findings contribute to a greater
understanding of when insects may be more active and foraging for nectar and pollen,
given the receptivity and biology of the flower in the earlier hours of the day.
Singh (1989) found that after Diptera, Coleopterans (beetles) were the most
numerous insects collected in his study, with 7 out of the 25 total insects belonging to
this order. Despite this small sample size, it offers a portrayal of perhaps other insects’
involvement in mango pollination aside from flies and bees. Similarly, our study
mirrored this and shed light on Cryptophagus sp. beetles and their interaction with
mango flowers. A total of 330 Cryptophagus sp., were collected, with similar numbers
collected in the morning, afternoon, and night, but mostly during weeks 6 and 7 of the
bloom period when fewer flowers were receptive.
Miridae and Thripidae captures increased significantly during the last two to three
weeks of bloom but are generally disregarded as important pollinators due to their pest
attributes and lack of abundance early in the blooming period. Although highly
abundant, these two insect families were almost exclusively found in one orchard, and
therefore act more as an outlier and not a good indicator of common species across
mango orchards. Orchard 2 had the most mirids and thrips, which may be due to
differences in cultural and pest control methods as further described below.
These results differ slightly from other studies, which could be a result of
collecting techniques influencing captures. All insects were collected with either a
sweep net on the inflorescence or a beat sheet, which favors crawling insects and may
42
lead to a collecting bias based on the insects’ behavior and speed at which it is able to
avoid collection. Another potential influence was the observation that some Syrphidae,
such as Copestylum violaceum, Palpada alhambra, and Ornidia obesa, were often seen
flying higher than other syrphids, roughly 6 feet up or higher and outside of our
collecting region. These 3 species were observed to be territorial and were far more
numerous than the data may suggest, especially in Orchard 2, but were outside of our
sampling area and were clumped in distribution. Futhermore, Muscidae, Calliphoridae,
and Syrphidae are quick to move and are difficult to catch with an insect sweep net.
Therefore, the fly numbers may be underrepresented in terms of how numerous they
are.
Differences in Orchards
All insects were collected in the same manner and with minimal bias, however all
three orchards varied in upkeep and maintenance. Differences between orchard
environments may not only impact insect diversity but the presence of key pollinators
during the bloom period. This is similar to findings from Carvalheiro et al. (2012) that
indicate the application of pesticides and seclusion from natural habitats lead to a
decrease in flying insects in mango orchards.
Orchard 1 is a non-commercial site with minimal insecticide use and limited
weeds. Mango trees were spaced 25’ x 25’ and the sides pruned to maintain an 8’
middle and tree height to maintain 15’, with open skies for plenty of sunlight to shine
through the canopy to reach branches and panicles lower down in the understory. The
greatest diversity of insects was found in Orchard 1, with low pest numbers at the end of
the blooming season.
43
Orchard 2 is a commercial orchard, with tall grasses, wild flowers, and weeds,
and has the greatest density of inflorescences amongst the three orchards when in
bloom. Although the data collected may not support it due to collecting difficulties,
Orchard 2 had the most observed Syrphidae present, perhaps due to having many
weeds infested with aphids that the syrphid larva could feed on. The trees were spaced
24’ x 24’ and pruned to maintain an open center (~8’ wide) and tree height of
~15’allowing sunlight to shine down through the canopy to the orchard floor. The
majority of pests were collected from Orchard 2, which resulted in most of the flowers
distorted and disfigured by weeks 7 and 8 from feeding by high populations of
Dagbertus sp. and Frankliniella sp.
Orchard 3 is a commercial orchard and was the most sprayed orchard, with
fungicides and insecticides applied weekly. The fewest insects were collected here,
possibly from the large amounts of insecticidal spraying and the limited number of
inflorescences. Tree density was greater than in the other sampled orchards, which
resulted in loss of much of the lower tree canopies and dense shade along the orchard
floor. All of the mango trees were connected and touching with over locking canopies,
leaving limited sunlight to shine through and limited branches and flowers in the
understory. Despite having 376 insects collected out of the total 4,564, Orchard 3 had
the highest population of Apis melifera and Drosophilidae. The prevalence of
honeybees was most likely due to the installation of managed honeybee hives in this
orchard. Especially prominent was Zaprionus sp., with the vast majority of specimens
collected at this site. In addition, all 18 Myllocerus undecimpustulatus were collected at
this site. There were limited weeds, grass and wild flowers. Interesting enough, despite
44
having far lower numbers of insects collected, this orchard had several insects not
found at other orchards. Several times no insects were found on multiple
inflorescences, followed by an inflorescence containing 20 or more flies clustered
together. This indicates perhaps a response to the lethal effects on insects in some
parts of the orchards and trees more heavily sprayed.
In conclusion, a wide diversity of insects visit mango flowers in south Florida and
there is a succession of insects throughout the mango bloom. Hippelates sp.,
Liohippelates sp., and Oscinella sp. were the most abundant insects during the first 3
weeks when mango flowering (i.e., the number of individual flowers opening).
Drosophilids, Sciarids, Cryptophagus sp., and Cicadellids were present across the
entire mango blooming period. Cardiastethus sp., Dagbertus sp., Microtechnites sp.,
Zaprionus sp., Frankliniella sp. were abundant during the last two weeks of the mango
bloom. Apis mellifera was rare in the three orchards. Differences in insect populations in
separate orchards suggest that cultural practices may affect populations of insects
visiting mango flowers.
45
Table 2-1. Insect sampling dates and times from Mangifera indica over the entire 8-week blooming period at three orchard sites in Miami-Dade County, Florida. Orchard 1 – (25°30’22.04” N 80°29’56.4 W); Orchard 2 – (25°29’50.15” N 80°29’25.64 W); Orchard 3 – (25°35’58.96” N 80°26’43.96 W).
Week Date Time
8-10 am 1-3 pm 8-10 pm 1 (1/23/18) Orchard 1 Orchard 1 Orchard 1
(1/24/18) Orchard 2 Orchard 2 (1/25/18) Orchard 3 Orchard 3 2 (1/30/18) Orchard 1 Orchard 1 Orchard 1
(1/31/18) Orchard 2 Orchard 2 (2/2/18) Orchard 3 Orchard 3 3 (2/6/18) Orchard 3 Orchard 3 (2/7/18) Orchard 1 Orchard 1 Orchard 1
(2/8/18) Orchard 2 Orchard 2 4 (2/13/18) Orchard 2 Orchard 2 (2/14/18) Orchard 3 Orchard 3 (2/15/18) Orchard 1 Orchard 1 Orchard 1
5 (2/21/18) Orchard 1 Orchard 1 Orchard 1
(2/22/18) Orchard 2 Orchard 2 (2/23/18) Orchard 3 Orchard 3 6 (2/27/18) Orchard 2 Orchard 2 (2/28/18) Orchard 3 Orchard 3 (3/1/18) Orchard 1 Orchard 1 Orchard 1
7 (3/6/18) Orchard 3 (3/7/18) Orchard 2 Orchard 2 (3/8/18) Orchard 1 Orchard 1 Orchard 1
8 (3/14/18) Orchard 2 Orchard 2 (3/16/18) Orchard 1 Orchard 1
46
Table 2-2. Total number of insects collected throughout the 8-week blooming period (23 January to 16 March 2018) from 3 mango (Mangifera indica) orchards in south Florida.
Orders Orchard 1 Orchard 2 Orchard 3
Araneae 90 33 14
Coleoptera 346 22 38
Collembola 1
Diptera 885 201 207
Hemiptera 204 518 44
Hymenoptera 47 107 30
Lepidoptera 18 21 9
Neuroptera 50 3 1
Odonata 1
Orthoptera 2
Psocoptera 4 1 1
Thysanoptera 160 1471 32
Trichoptera 3
Grand Total 1811 2377 376
47
Table 2-3. Insects most prevalent throughout the 8-week mango blooming period (Jan. 23 to March 16, 2018) at 3 mango orchards in south Florida. Orchard numbers represent total caught, while numbers under time of day and weeks are percent.
Percent Per Week Orchards
Family Species Total Insects % Morning % Afternoon% Night 1 2 3 4 5 6 7 8 Orchard 1Orchard 2Orchard 3
Curculionidae Myllocerus
undecimpustulatus 18 55.6 44.4 0.0 0.0 27.8 22.2 11.1 5.6 33.3 0.0 0.0 0 0 18
Cryptophagidae Cryptophagus sp. 330 29.1 33.9 37.0 2.4 0.0 10.9 17.3 5.2 30.6 29.7 3.9 302 13 15
Calliphoridae complex 4 25 75 0 25 0 0 50 0 25 0 0 2 2 0
Ceratopogonidae Forcipomyia sp. 1 100 0 0 100 0 0 0 0 0 0 0 1 0 0
complex 136 31 31 38 6 28 15 7 6 21 10 7 97 28 11
Chloropidae Ceratobarys sp. 15 73 27 0 47 0 27 0 27 0 0 0 14 1 0
Hippelates sp. 246 72 25 3 61 11 17 1 5 2 2 1 187 20 39
Liohippelates sp. 301 60 39 1 14 19 46 9 10 2 1 0 230 32 39
Oscinella sp. 121 31 31 38 10 50 21 6 10 3 0 0 106 12 3
Drosophilidae Drosophila sp. 74 65 30 5 1 0 9 19 14 14 41 3 9 41 24
Zaprionus indianus 28 93 4 4 0 0 0 4 0 75 21 0 1 0 27
complex 66 85 5 11 15 33 45 2 2 3 0 0 16 6 44
Muscidae Atherigona reversura 7 14 43 43 0 0 14 14 0 14 0 57 3 4 0
complex 14 50 29 21 7 29 14 7 7 7 0 29 7 5 2
Sciaridae complex 132 14 7 80 5 2 7 62 2 12 8 2 121 11 0
Syrphidae Allograpta obliqua 4 50 25 25 0 0 0 50 50 0 0 0 3 1 0
Copestylum violaceum 1 0 100 0 0 0 0 100 0 0 0 0 0 1 0
Ornidia obesa 1 100 0 0 100 0 0 0 0 0 0 0 0 0 1
Palpada mexicana 2 100 0 0 0 0 0 50 50 0 0 0 1 1 0
Toxomerus marginatus 3 100 0 0 0 0 33 0 67 0 0 0 3 0 0
complex 2 0 100 0 0 50 0 0 0 50 0 0 1 0 1
Anthocoridae Cardiastethus sp. 31 38.7 61.3 0.0 0.0 0.0 0.0 0.0 0.0 6.5 77.4 16.1 0 31 0
Aphididae complex 56 57.1 25.0 17.9 17.9 1.8 23.2 7.1 7.1 25.0 14.3 3.6 24 9 23
Cicadellidae complex 152 25.0 34.2 40.8 9.2 3.3 34.2 22.4 7.9 10.5 8.6 3.9 101 42 9
Miridae Camplyomma verbasci 27 63.0 37.0 0.0 0.0 0.0 0.0 0.0 0.0 0.0 22.2 77.8 0 27 0
Dagbertus sp. 304 57.2 41.4 1.3 0.0 0.0 0.0 0.0 0.3 0.0 36.8 62.8 10 294 0
Microtechnites bractatus 15 46.7 53.3 0.0 0.0 0.0 6.7 6.7 6.7 0.0 60.0 20.0 10 4 1
complex 98 56.1 38.8 5.1 10.2 17.3 6.1 6.1 13.3 8.2 38.8 0.0 33 60 5
Apidae Apis mellifera 12 66.7 33.3 0.0 8.3 33.3 25.0 8.3 25.0 0.0 0.0 0.0 1 4 8
Braconidae complex 18 27.8 33.3 38.9 0.0 0.0 16.7 44.4 0.0 0.1 16.7 11.1 10 4 4
Eulophidae Quadrastichus sp. 12 41.7 58.3 0.0 0.0 0.0 41.7 16.7 0.0 0.4 0.0 0.0 0 11 1
complex 33 39.4 48.5 12.1 0.0 12.1 3.0 9.1 15.2 0.1 24.2 27.3 7 26 0
Thripidae Frankliniella occidentalis 1643 65.7 31.8 2.6 0.1 0.0 0.1 0.0 0.0 1.6 27.8 70.4 152 1460 31
48
Table 2-4. The percentage of Diptera collected throughout the 8-week blooming period (23 January to 16 March 2018) in 3 mango orchard locations in south Florida by time of day and week.
Percent Per Week
Family Species % Morning % Afternoon% Night 1 2 3 4 5 6 7 8
Agromyzidae Ophiomyia sp. 1 100 0 0 0 0 0 0 0 0 100 0
unidentfied 4 25 50 25 0 0 0 50 0 25 0 25
Calliphoridae complex 4 25 75 0 25 0 0 50 0 25 0 0
CeratopogonidaeForcipomyia sp. 1 100 0 0 100 0 0 0 0 0 0 0
complex 136 31 31 38 6 28 15 7 6 21 10 7
Chironomidae Tanytarsus sp. 9 56 11 33 0 0 0 0 22 67 11 0
complex 17 6 12 82 0 12 65 0 12 12 0 0
Chloropidae Ceratobarys sp. 15 73 27 0 47 0 27 0 27 0 0 0
Hippelates sp. 246 72 25 3 61 11 17 1 5 2 2 1
Liohippelates sp. 301 60 39 1 14 19 46 9 10 2 1 0
Oscinella sp. 121 31 31 38 10 50 21 6 10 3 0 0
complex 15 40 60 0 0 13 0 60 13 7 0 7
Chyromyidae complex 4 25 0 75 0 75 0 25 0 0 0 0
Culicidae complex 2 0 50 50 0 0 0 50 0 50 0 0
Drosophilidae Drosophila sp. 74 65 30 5 1 0 9 19 14 14 41 3
Scaptomyza sp. 1 100 0 0 0 0 0 0 0 100 0 0
Zaprionus indianus 28 93 4 4 0 0 0 4 0 75 21 0
complex 66 85 5 11 15 33 45 2 2 3 0 0
Ephydridae Leptopsilopa sp. 1 0 0 100 0 0 100 0 0 0 0 0
Notiphila sp. 1 100 0 0 0 0 0 100 0 0 0 0
complex 15 47 40 13 0 13 27 7 13 13 7 20
Fanniidae complex 1 0 100 0 100 0 0 0 0 0 0 0
Lauxaniidae Camptoprosopella sp. 1 100 0 0 0 0 0 0 100 0 0 0
complex 1 0 100 0 0 0 0 0 0 0 0 100
Limoniidae complex 1 0 0 100 0 0 0 0 0 100 0 0
Micropezidae complex 1 100 0 0 0 0 100 0 0 0 0 0
Muscidae Atherigona reversura 7 14 43 43 0 0 14 14 0 14 0 57
complex 14 50 29 21 7 29 14 7 7 7 0 29
Phoridae complex 4 0 75 25 0 0 25 0 25 25 25 0
Sarcophagidae complex 4 25 50 25 0 0 0 25 25 50 0 0
Sciaridae Odontosciara sp. 1 100 0 0 0 0 0 0 0 0 0 100
complex 132 14 7 80 5 2 7 62 2 12 8 2
Syrphidae Allograpta obliqua 4 50 25 25 0 0 0 50 50 0 0 0
Copestylum violaceum 1 0 100 0 0 0 0 100 0 0 0 0
Ornidia obesa 1 100 0 0 100 0 0 0 0 0 0 0
Palpada mexicana 2 100 0 0 0 0 0 50 50 0 0 0
Toxomerus marginatus 3 100 0 0 0 0 33 0 67 0 0 0
complex 2 0 100 0 0 50 0 0 0 50 0 0
Tephritidae Dioxyna picciola 1 0 100 0 0 0 0 100 0 0 0 0
Evaresta 1 0 100 0 0 0 0 100 0 0 0 0
Xanthaciura sp. 7 43 57 0 0 0 14 0 0 71 14 0
complex 1 100 0 0 100 0 0 0 0 0 0 0
Tipulidae complex 10 10 10 80 0 40 20 0 10 30 0 0
Ulidiidae Seioptera sp. 1 0 100 0 0 100 0 0 0 0 0 0
complex complex 29 48 10 41 14 48 7 3 21 3 3 0
Total
Insects
49
Table 2-5. The percentage of Coleoptera collected throughout the 8-week blooming period (23 January to 16 March 2018) in 3 mango orchard locations in south Florida by time of day and week.
Percent Per Week
Family Species % Morning % Afternoon% Night 1 2 3 4 5 6 7 8
Chrysomelidae Cryptocephalus irroratus 2 50 50 0 0 0 0 0 0 50 50 0
Diabrotica balteata 1 100 0 0 100 0 0 0 0 0 0 0
Diachus auratus 2 100 0 0 0 0 0 0 0 0 0 100
Coccinellidae Brachiacantha sp. 1 0 100 0 0 0 0 0 100 0 0 0
Cycloneda sanguinea 3 67 33 0 0 0 0 0 0 33 67 0
Delphastus sp. 2 0 100 0 0 0 0 100 0 0 0 0
Diomus sp. 3 100 0 0 0 0 0 0 0 33 67 0
Harmonia axyridis 2 100 0 0 0 0 0 50 0 0 50 0
Scymnus sp. 2 0 100 0 0 0 0 0 50 0 50 0
complex 9 22 44 33 11 0 11 0 22 44 11 0
Cryptophagidae Cryptophagus sp. 330 29 34 37 2 0 11 17 5 31 30 4
complex 5 40 40 20 20 20 20 20 0 0 20 0
Curculionidae Diaprepes abbreviatus 1 0 100 0 100 0 0 0 0 0 0 0
Hypothenemus sp. 2 50 0 50 0 0 0 0 50 50 0 0
Myllocerus
undecimpustulatus
18 56 44 0 0 28 22 11 6 33 0 0
Scolytinae sp. 1 100 0 0 0 0 0 0 0 100 0 0
complex 6 33 33 33 0 17 50 17 0 17 0 0
Kateretidae complex 1 100 0 0 0 0 0 100 0 0 0 0
Latridiidae Melanophthalma sp. 6 0 67 33 0 0 0 17 0 17 67 0
complex 2 0 100 0 0 0 0 0 50 50 0 0
Scarabeidae Euphoria sepulcralis 3 0 33 67 0 0 0 33 33 33 0 0
complex 1 100 0 0 0 0 100 0 0 0 0 0
Staphylinidae complex 3 33 33 33 0 0 67 0 0 0 33 0
Total
Insects
50
Table 2-6. The percentage of Hemiptera collected throughout the 8-week blooming period (23 January to 16 March 2018) in 3 mango orchard locations in south Florida by time of day and week.
Percent Per Week
Family Species % Morning % Afternoon% Night 1 2 3 4 5 6 7 8
Anthocoridae Amphiareus sp. 2 0 0 100 0 0 0 0 0 100 0 0
Cardiastethus sp. 31 39 61 0 0 0 0 0 0 6 77 16
Orius sp. 10 40 60 0 20 0 0 0 20 10 20 30
complex 6 83 17 0 0 17 17 0 0 0 17 50
Aphididae Tetraneura sp. 1 0 100 0 0 0 100 0 0 0 0 0
complex 56 57 25 18 18 2 23 7 7 25 14 4
Cercopidae complex 8 63 38 0 0 25 38 13 13 13 0 0
Cicadellidae Protalebrella brasiliensis 5 20 60 20 0 20 0 0 0 0 80 0
complex 152 25 34 41 9 3 34 22 8 11 9 4
Delphacidae complex 21 38 52 10 0 0 29 5 10 19 19 19
Flatidae Ormenoides sp. 1 100 0 0 0 0 0 0 0 0 100 0
Geocoridae complex 1 100 0 0 100 0 0 0 0 0 0 0
Lygaeidae complex 1 100 0 0 100 0 0 0 0 0 0 0
Miridae Campylomma verbasci 27 63 37 0 0 0 0 0 0 0 22 78
Dagbertus sp. 304 57 41 1 0 0 0 0 0 0 37 63
Lygocoris sp. 3 67 33 0 67 0 0 0 0 0 0 33
Microtechnites bractatus 15 47 53 0 0 0 7 7 7 0 60 20
Pcynoderes sp. 9 0 100 0 0 0 0 0 0 0 33 67
complex 98 56 39 5 10 17 6 6 13 8 39 0
Pentatomidae Proxys punctualis 1 0 100 0 0 0 0 0 0 0 100 0
Psyllidae complex 2 100 0 0 0 100 0 0 0 0 0 0
Reduviidae complex 3 33 67 0 0 0 0 33 0 33 0 33
Rhyparochromidae complex 2 0 0 100 0 0 0 50 50 0 0 0
Blank complex 6 50 50 0 33 0 0 17 0 0 17 33
Total
Insects
51
Table 2-7. The percentage of Hymenoptera collected throughout the 8-week blooming period (23 January to 16 March 2018) in 3 mango orchard locations in south Florida by time of day and week.
Percent Per Week
Family Species
Total
Insects % Morning % Afternoon% Night 1 2 3 4 5 6 7 8
Apidae Apis mellifera 12 67 33 0 8 33 25 8 25 0 0 0
Unidentified 1 100 0 0 0 100 0 0 0 0 0 0
Apocrita complex 3 0 100 0 0 0 0 0 33 0 0 33
Braconidae complex 18 28 33 39 0 0 17 44 0 0 17 11
Chalcidoidea complex 1 0 100 0 0 0 0 100 0 0 0 0
Encyrtidae Enyrtus sp. 1 100 0 0 0 0 0 100 0 0 0 0
Eulophidae Quadrastichus sp. 12 42 58 0 0 0 42 17 0 0 0 0
complex 33 39 48 12 0 12 3 9 15 0 24 27
Figidae Aganaspis sp. 1 100 0 0 100 0 0 0 0 0 0 0
Ealata sp. 1 0 100 0 100 0 0 0 0 0 0 0
complex 1 0 100 0 100 0 0 0 0 0 0 0
Formicidae Brachymyrmex sp. 11 9 91 0 0 0 36 0 0 0 0 45
Camponotus floridanus 1 0 0 100 0 0 0 0 0 1 0 0
Pheidole sp. 25 72 28 0 0 0 0 20 4 0 72 0
Pseudomyrmex gracilis 2 50 50 0 0 0 0 50 0 0 0 50
Tapinoma melanocephalum 7 29 71 0 0 0 0 0 0 0 100 0
Technomyrmex difficilis 2 0 0 100 0 0 0 0 0 1 0 0
complex 17 47 47 6 35 24 18 6 6 0 0 6
Halictidae complex 1 100 0 0 0 0 0 0 0 1 0 0
Ichneumonidae complex 4 25 25 50 0 0 0 0 50 0 50 0
Pteromalidae complex 4 25 75 0 0 0 0 50 50 0 0 0
Unidentified complex 26 35 62 4 19 12 4 15 8 0 19 8
52
Table 2-8. The percentage of Thysanoptera collected throughout the 8-week blooming period (23 January to 16 March 2018) in 3 mango orchard locations in south Florida by time of day and week.
Percent Per Week
Family Species % Morning % Afternoon% Night 1 2 3 4 5 6 7 8
Aeolothripidae Franklinothrips vespiformis 2 100 0 0 0 0 0 0 0 100
complex 1 100 0 0 0 0 0 100 0 0
Phlaeothripidae complex 8 38 50 13 0 0 0 13 0 13 63 13
Thripidae Frankliniella occidentalis 1643 66 32 3 0 0 0 0 0 2 28 70
complex 4 75 25 0 0 0 0 0 0 50 50 0
complex complex 5 40 40 20 40 20 20 0 0 0 0 20
Totat
Insects
53
Figure 2-1. Orchard 1 (25°30’22.04” N 80°29’56.4 W) on January 1, 2018, during the beginning of panicle emergence.
Photo courtesy of Matthew Quenaudon.
54
Figure 2-2. Orchard 2 (25°29’50.15” N 80°29’25.64 W) a commercial orchard on February 13, 2018, during the
completion of panicle emergence and flower opening. Photo courtesy of Matthew Quenaudon.
55
Figure 2-3. Orchard 3 (25°35’58.96” N 80°26’43.96 W), commercial orchard on January 25, 2018, during early panicle
emergence and flowering which was sparse. Orchard 3 had a heavy canopy with limited inflorescence in the understory. Photo courtesy of Matthew Quenaudon.
56
Figure 2-4. Most abundant insect orders collected from three mango orchards in south Florida during the 2018 8-week blooming period in south Florida from 23 January to 16 March 2018.
57
Figure 2-5. The five most prevalent Dipteran families collected on Mangifera indica throughout the 8-week blooming period across the three orchards in south Florida.
58
Figure 2-6. Comparison of the four most prevalent Chloropidae genera collected from three mango (Mangifera indica) orchards in south Florida during the 2018 8-week blooming period (23 January to 16 March) based on the time of day. Nighttime collections were only conducted at one location (TREC) for the first 7 weeks.
59
Figure 2-7. Comparison of the two most prevalent Chloropidae genera collected from three mango (Mangifera indica) orchards in south Florida from 23 January to 16 March 2018.
60
CHAPTER 3 INSECT BEHAVIOR AND POLLEN COLLECTION DURING FLOWER VISITATIONS
Introduction
The morphology of an insect and its behavioral interactions with flower sexual
organs help form an understanding of how important an insect may be in contributing to
successful pollination. Many scientists believe efficient pollinators have a high
population density and are in constant movement between flowers resulting in a high
frequency of interaction (Rader et al., 2009). The problem with determining which
insects fit this narrative in mangoes stems from the ambiguity in determining which
flowers are visited because of the small size of mango flowers (Huda et al., 2015). Prior
to looking at the duration and interaction of an insect on a flower, it is important to
comprehend the insect’s behavior.
The behavior of an insect is considered an important factor in pollen deposition
success, and influences whether pollen comes into contact with the stigma. Insect
behavior differs among orders, families, and species so it is important to determine
which insects are visiting the flowers. For example, ants (Formicidae) are present in
both frequency and density on mango but are often viewed as poor pollinators because
ants have little to no interaction with the stigma (Huda et al., 2015). In addition, ants
have grooming habits, which possibly remove any pollen adhering to their body. In
addition, the presence of ants often discourages other insects such as small flies from
visiting the flower (Huda et al., 2015). Understanding these small subtleties will help
define key pollinators and further pollination research.
Another aspect of behavior includes the duration and interaction of the most
prevalent insects with floral sexual organs on mango flowers. Although visitation rate is
61
divided into two parts: 1. how often an individual is observed on a flower per unit time;
and 2. how many individuals per flower are present per unit of time (Ne’eman et al.,
2010), this does not include the insects’ interaction with the flower’s sexual organs,
which is vital to ensuring pollination. As previously discussed, visitation frequency and
population density can be important indicators of valuable pollinators but understanding
behavior on the flower can provide knowledge as to whether they are actually
contributing to pollination. Monzon et al. (2004) determined that the behavior of an
important mason bee pollinator of pear, Osmia cornuta, directly affects pollination.
Osmia cornuta repeatedly landed on the reproductive structures of pear flowers
gathering pollen from anthers while moving their proboscis around in search of nectar.
In another study looking at the importance of bees, Peponapis pruinosa, on summer
squash (Cucurbita pepo), it was determined that males visited flowers twice as
frequently as the female bees, thereby increasing their role in pollination (Cane et al.,
2011. These studies both demonstrate how differences in behavior may play a role in
pollination and the value of understanding the contribution of behavior of the species
being observed.
Another important aspect for successful pollination, is the amount of pollen an
insect can carry and deposit. If consistent contact with the stigma is occurring and
pollen is present, there is a good chance for pollination and subsequent fertilization.
Estimating how much pollen an insect may be depositing on a mango inflorescence can
be difficult to determine due to the small flower size. Howlett et al. (2011) concluded
that collecting an insect directly from a flower and measuring the quantity of pollen
grains on its body is an easy, fast, and accurate technique to gage pollen carrying
62
capacity and deposition. The amount of pollen an insect can carry can depend on
multiple factors, including larger abdominal surface size, tongue length, presence of a
scopa, hairiness, and grooming behavior (Willmer and Finlayson, 2014).
In this study we hypothesize that insects of larger size will carry higher amounts
of pollen as shown in previous studies (Huda et al., 2015) and that Diptera will be
important pollinators based on past research (Sung et al., 2006; Huda et al., 2015;
Kumar et al., 2016). Although Apis mellifera is considered a key pollinator of mangoes
in Sao Francisco, Brazil, Diptera are the primary pollinators of mango in other tropical
areas (Ramirez and Davenport, 2016). The objective of this study was to determine
three different aspects of pollinator importance: (1) the behavior of the most common
arthropods during mango flower visitation; (2) duration and interaction with flowers and
flower structures; and (3) the amount of mango pollen transported.
Materials and Methods
A mango orchard, Mangifera indica ‘Keitt’, located at the Tropical Research and
Education Center (TREC) was selected to determine the number of arthropod visits to
mango flowers, observation of visiting behavior, and identification of those arthropods.
Observational data of insects visiting flowers were recorded in a different year than
when insects were collected for pollen quantification. The observational data were
collected between March 4 and April 20, 2018, during a second flush of newly formed
inflorescences, whereas insects collected for pollen determination were collected
between February 5 to 7, 2019. Trees were selected based on their availability of
inflorescences with pollen receptive flowers. At this time of year, there were only a few
trees with new inflorescences blooming within the same area. Over the course of 6
weeks, inflorescences with flower blooms on these selected trees were used for
63
observational field studies. Observations were conducted every other day in the
morning between 8 and 11 am or in the afternoon from 1 to 3 pm when insect activity
was at its peak and flowers were still receptive.
Once an insect was present on an inflorescence, it was observed for up to 2
minutes or until the insect flew away and could no longer be observed. Flowers
observed were those recently opened or considered receptive for pollination. During
that time the number of flowers visited and the insect's behavior and interaction with the
flower was recorded. Behavior data collected included movement speed, flight pattern,
if the insect groomed itself, and interaction with other insects. Insect visit duration per
flower and whether nectar or pollen was fed on or collected were recorded. Insects
found feeding on the outside portion of the flowers were marked as foraging on pollen
while those positioned in the middle were marked as foraging on nectar. Assumption of
foraging behavior based on the location of the insects on the flowers was due to
observations of where pollen and nectar are located within mango flowers. In our
observations, nectar was observed closer to the middle of the flower near the floral
disks, whereas pollen was found gathered near the edges of the flower. Insects
observed feeding between the two locations were marked as both. After the 2-minute
observation, the insect was collected using a kill jar and immediately placed in a vial
following death with minimal contact. At times, the insect was not able to be collected.
Collected insects were frozen at -20°C and held for further identification and pollen
acquisition at TREC.
For pollen quantification, frozen insects were thawed for 15 minutes after which
they were submerged in 50 microliters of 70% ethanol and vortexed for 30 seconds in
64
micro-centrifuge tubes to wash off any pollen. The same procedures were used for all
insects with the exception of A. mellifera, where the corbicula was removed prior to
washing the specimen. Removal of the corbicula is a standard practice for studies
involving pollination success, due to the pollen found in the corbicula being unavailable
for pollination services (Delaplane et al., 2013). Ten microliters were immediately
removed from the solution and pipetted into a haemocytometer for counting. The insect
was vortexed for another 30 seconds before a second extraction of 10 microliters was
placed into the second loading section of the haemocytometer. The insect and the
remaining 30 microliters were then labeled and kept for further analysis.
Transmitted light microscopy was used for pollen identification. The number of
mango pollen grains per insect sample was counted. Mango pollen was distinguished
from other pollen grains by comparing with samples directly derived from mango
flowers. Due to the relatively low number of pollen grains, nine alternating squares of
the haemocytometer were counted. If no pollen grains were in these 9 squares, the
number of pollen grains in the entire 10 microliter sample was counted. The insect was
identified prior to pollen collection, and the number of pollen grains for each insect was
recorded with the date collected.
Results
Eight different genera of insects were observed visiting mangoes between March
4 and April 20, 2018. With a few exceptions, insect identification during observations
were to the family level which included the Chloropidae, Syrphidae, Muscidae,
Sciaridae, and Calliphoridae. Individuals identified to genus or species included Apis
mellifera, Brachymyrmex sp., and Camponotus floridanus.
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The insects observed and the average number of flowers visited, average time
spent on each flower, total number of individuals collected, total number of flowers
visited, and number of visits for pollen and nectar were tabulated (Table 3-1). Most
insects observed foraged on pollen and nectar and include the Chloropidae, Syrphidae,
and Musicdae whereas insects from the remaining families mostly foraged on pollen
alone.
The smallest of the insects observed (Sciaridae, Chloropidae, and
Brachymyrmex sp.) were also the 3 insects with the lowest average number of flowers
visited per 120 seconds (Figure 3-1). Sciaridae visited the least number of flowers with
an average of 1.09 flowers per 120 seconds. These insects were often found stationary
or moving slowly around and inside mango flowers feeding on both pollen and nectar. In
comparison, larger insects moved quickly amongst the flowers with Camponotus
floridanus averaging 7.16 flowers per 120 seconds. This, however, may be skewed
slightly as these ants were almost always observed for the full 120 seconds, due to their
inability to fly away upon approach. Although the muscids and A. mellifera averaged
3.56 and 4.60 flowers per visitation, respectively, they moved more quickly and thus
were almost never observed for a full 120 seconds as the observers lost sight of them
before the period was done.
Apis mellifera was recorded to have the lowest interaction time with mango
flowers, averaging 42 seconds per visit, which in contrast to Brachymyrmex sp., that
were observed on a single flower for the full 120 seconds (Figure 3-2). However, a low
number (5) of honey bees were observed. Other insects observed for longer periods of
time included Camponotus floridanus, Chloropidae, and Sciaridae, which were also
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those groups that had the fewest numbers of flowers visited on average per 120 second
observation period. Insect activity was correlated with the size of the insect. Smaller
insects may be more likely to remain stationary while feeding while larger insects moved
quickly and frequently amongst flowers.
From Feb 5 to 7, 2019, 1 to 9 insects of 15 species of insects were collected from
mango flowers for pollen quantification. These species include Brachiacantha barberi,
Cryptophagus sp., Euphoria sepulcralis, Hippelates sp., Liohippelates sp., Oscinella sp.,
Chrysotus sp., Ephydridae, Muscidae, Platypeza sp., Sarcophagidae, Sciaridae,
Allograpta obliqua, Apis mellifera, and Camponotus planatus.
Apis mellifera had pollen counts greater than any other insect collected,
averaging 788 pollen grains per insect (Table 3-2). Muscids averaged 47 pollen grains
per insect, followed by the syrphid, Allograpta oblique, with an average of 16 pollen
grains per insect. Camponotus planatus averaged 15 pollen grains followed by
Sarcophagidae averaging 14.6. Insects with an average of less than 10 pollen grains
per insect included two different beetles, Euphoria sepulcralis and Brachiacantha
barberi and 3 flies, Ephydridae, Hippelates sp., and Oscinella sp.
Chloropidae and Sciaridae displayed similar behavior characteristics of time
spent on the flower. These insects were found to move between the petals and the
ovary, with their abdomen rubbing up against any anthers present while searching for
nectar amongst the floral disks. Chloropidae moved at a brisk pace, whereas Sciaridae
moved leisurely amongst the flowers. Grooming habits were not observed, and insects
were viewed several times flying away upon intrusion by larger insects such as muscids
or Camponotus floridanus.
67
Muscidae and Calliphoridae were often seen zipping between flower to leaf and
resting on nearby leaves. Muscidae were observed grooming their legs on occasion
and both insects were sporadic with their movement. Interaction with other insects was
rarely noted. Muscids would often be found landing on the edge of the flower, with its
legs on the petals and outer boundary of the flower. The dorsal side of the abdomen
could be viewed contacting the reproductive structures of the flower. Syrphids were
typically smaller and would touch down briefly on a flower often landing on the edge or
middle of the flower. With smaller legs, syrphids appeared down in the flower, rubbing
up against the stamen and stigma. Syrphid flight behavior can be compared to a
helicopter, often hovering in place a few inches to a few feet from a potential flower,
before carefully landing and either moving from flower to flower or flying back into the
air. Not as quick as the calliphorids or muscids, syrphids were the most hesitant in
approaching a flower.
Apis mellifera was seldom seen on mangoes during observation and were quick
to fly away. A. mellifera lacked interest in flowers despite the hundreds of available
flowers for nectar or pollen collecting and would roam around flowers before dispersing
to some other location. Brachymyrmex sp. are much smaller than C. floridanus and
would often be found moving slowly within the mango flowers whereas C. floridanus
were actively moving from flower to flower. Brachymyrmex sp. favored feeding near the
floral disks, presumably feeding on nectar while C. floridanus was observed feeding on
the edges of the flower where potential pollen may have fallen. C. floridanus were often
territorial while feeding, causing other insects to leave or fly away when approached.
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Discussion
Further insight into the primary insects visiting mango flowers, Mangifera indica,
in the south Florida region and the amount of pollen each may be carrying was explored
in this chapter. An observational approach provides an opportunity to identify those
insects associated with mangoes that may have been missed with a sweep net. Similar
to Huda et al. (2015) observations of 5 insect genera pollinating mangoes in Malaysia,
our findings show similar insects, including Camponotus sp., Sarcophaga sp.,
Calliphoridae, and Brachymyrmex sp. This coincides with another report from southern
Taiwan, where 15 species were found visiting mango flowers of which 42% were
Diptera (Sung et al., 2006).
Although Apis mellifera may carry the most pollen grains, it is often the flies that
are most prevalent and found on mango inflorescences. The lack of honeybees, sweat
bees, and other solitary bees visiting mango flowers in this study demonstrates that
either bees are not attracted to mango flowers or that other factors play a role in the
shortage of Hymenoptera within mango orchards. These data agree with other reports
that Diptera are the most prevalent and important insects in mango orchards, whether it
be Syrphidae and Bombyliidae (Kumar et al., 2016), Chrysomya megacephala and
Musca domestica (Sung et al., 2006), or Eristalinus sp. and Stomorhina sp. (Huda et al.,
2015).
Insect morphology and size appear to influence the average time an insect visits
an individual flower. Average flower visit time seemed to increase as body size of the
insect decreased. Smaller insects such as Sciaridae, Chloropidae, and Brachymyrmex
sp. averaged the fewest flowers visited per observation period (120 seconds) indicating
their slow movement while navigating the mango flowers (Figure 3-1). This is indicative
69
of the potential attractiveness and/or size compatibility of mango flowers as well as
general insect mobility and behavior. Larger insects such as Muscidae, Apis mellifera,
Syrphidae, Calliphoridae, and Camponotus floridanus averaged more flowers per visit in
the 120 seconds demonstrating their active behavior while foraging. Depending on the
morphology of the insect and interaction of its appendages with the anthers or stamen,
this can be a benefit or detriment to pollination efficiency.
Long visitation time may result in greater pollen deposition rates, however, less
visits per time could result in less cross pollination. Body size and how the pollen is
stored on an insect are also factors that play a role in pollination. A large insect for
instance, will not fit inside a small mango flower allowing it to touch the stigma or anther.
In this case, it would be important that pollen adheres to an insect’s legs or ventral side
of the abdomen if that is the only part of the body contacting plant reproductive parts.
Similarly, a very small insect may spend minutes in one flower but never contact any
pollen or the stigma while feeding on nectar. Insect setae help pollen adhere to the
body or appendages of an insect and are key factors in how successful an insect may
be in the transfer of pollen. Future observational studies based on insect size could
further elaborate which insects may be efficient pollinators of mangoes due to the
morphological traits that are associated with different pollinators.
Although it has been reported that smaller ants such as Iridomyrmex sp. carry
very few pollen grains on their body; larger ants such as Camponotus sp. have been
reported to be key participants in mango pollination (Huda et al., 2015). Camponotus
planatus averaged 15 pollen grains per sample, which was roughly equivalent to both
the Sarcophagidae and Allograpta obliqua pollinators that carried 14.6 and 16 pollen
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grains on average, respectively. The variance in insects collected suggests the best
pollinators for each orchard may differ due to location. This is to suggest each orchard
may have different insect pollinators better suited for it’s specific geography and climate.
Based on the collective data from observations, behavioral traits, and pollen
carrying capacity, the insects of most importance include Syrphidae, specifically A.
oblique, Muscidae, Sarcophagidae, Drosophila sp., Cryptophagus sp., Camponotus
planatus, Hippelates sp., Liohippelates sp., and Ceratopogonidae. Most of these
insects have been shown to carry mango pollen and those that haven’t are extremely
prevalent and need to be further looked at to demonstrate their importance in mango
pollination. Although most insects collected in our insect diversity study (Chapter 2)
were present in our observational and pollen quantification studies, there were a few
insects that were not caught that could be of importance in pollination. The ants, in
particular Brachymyrmex, Camponotus floridanus, and Camponotus planatus were
extremely prevalent during our observational and pollen quantification studies but were
seldom collected with sweep net sampling. However, an ant that was present during
our sweet net sampling, Pheidole sp., was not present during our observational study.
Most of the larger flies were often seen during our sampling but seldom collected in
sweep nets, whereas these insects were better represented during our observational
and pollen study. On the flipside, smaller flies such as Sciaridae, Ceratopogonidae, and
Drosophila were commonly collected during our sweep net sampling but not in the
observational study likely due to difficulty in seeing these small insects.
Method of insect sampling influenced the number and diversity of insects
collected on mangoes. In order to better understand the insects of most importance in
71
mango pollination, it is important to consider multiple methods of insect collection.
Number of samples and sample size also influences the number and diversity of insects
collected. Increasing either of these will provide increased accuracy and help pinpoint
the most effective pollinators of mangoes. The number of insects collected in this study
was low and observations were only conducted during one bloom season for a few days
during each sample week. This brief sampling period could lead to a bias in the insects
collected based on what insects are present during that timeframe. Increased sampling
across multiple orchards and over multiple blooming seasons could strengthen the data
and provide improved insight on the key pollinators of mangoes.
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Table 3-1. Observed insects on ‘Keitt’ mango flowers (Mangifera indica) from March 4 to April 20, 2018 at the Tropical Research and Education Center, Homestead, Florida.
Insect
Avg Number Of
Flowers
Visited per 2 min
Average Time
Per
Visit (sec)
Total # of
Insects
Observed
Total # of
Flowers
Visited
Pollen
Collecting / Feeding
(# of insects)
Nectar Collecting
/ Feeding (# of
insects)
Pollen & Nectar
Collecting / Feeding
(# of insects)
Chloropidae 1.25 ± 0.07 112.91 ± 3 55 69 54 12 11
Syrphidae 5.03± 0.45 103.81 ± 6 31 156 30 23 22
Muscidae 3.56 ± 0.40 96.92 ± 5 39 139 38 15 14
Apis mellifera 4.6 ± 0.54 42 ± 20 5 23 5 1 1
Sciaridae 1.09 ± 0.09 110 ± 21 10 12 10 1 1
Calliphoridae 5.38 ± 0.55 109.52 ± 8 21 113 21 2 2
Brachymyrmex sp. 1.65 ± 0.16 120 ± 0 23 38 23 1 1
Camponotus floridanus 7.15 ± 0.66 118.95 ± 6 19 136 19 3 3
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Table 3-2. Quantification of mango (Mangifera indica) pollen on insects collected from ‘Keitt’ mango trees from Feb 5 and Feb 7, 2019 at the Tropical Research and Education Center, Homestead, Florida.
InsectTotal Insects
Collected
Mean Number (±SE) of
Pollen Grains Per Insect
Total Pollen Grains
Counted
Brachiacantha barberi 5 3.7 ± 3.38 37
Cryptophagus sp. 1 0 0
Euphoria sepulcralis 2 7.5 ± 7.03 30
Hippelates sp. 1 1 ± 1.41 2
Liohippelates sp. 2 0 0
Oscinella sp. 6 0.33 ± 0.36 4
Chrysotus sp. 1 0 0
Ephydridae 1 3 ± 2.83 6
Muscidae 9 46.83 ± 20.96 843
Platypeza sp. 1 0 0
Sarcophagidae 4 14.625 ± 9.09 117
Sciaridae 1 0 0
Allograpta obliqua 6 16.17 ± 5.31 194
Apis mellifera 4 788.25 ± 209.49 6306
Camponotus planatus 3 15.33 ± 8.43 92
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Figure 3-1. The mean number of flowers visited on ‘Keitt’ mango (Mangifera indica) at the Tropical Research and Education Center, Homestead, Florida, during a 120 second visual observation from March 4 and April 20, 2018.
75
Figure 3-2. The mean visual observation time insects visited ‘Keitt’ mango (Mangifera
indica) inflorescences up to 120 second time period from March 4 to April 20, 2018 at the Tropical Research and Education Center, Homestead, Florida.
76
CHAPTER 4 IMPORTANCE OF ARTHROPODS IN POLLINATION AND FRUIT SET AND
PRODUCTION OF MANGIFERA INDICA
Introduction
The significance of insects and the impact they have on pollination in agricultural
landscapes has been researched and further supports the ways in which non-managed
insects increase fruit set. A total of 41 crop systems worldwide revealed a positive
correlation of fruit set with wild insects (Garibaldi et al., 2013). They concluded that wild
insects more effectively pollinated crops than did honey bees, boosting fruit set by up to
twice as much. In addition, results indicate that lack of wild pollinator species richness
leads to a decrease in visitation from these wild insects and lower fruit set quantities
(Garibaldi et al., 2013). Therefore, to attribute a single species as a main pollinator or
justify augmenting a population of honeybees for a select crop is continuously revealed
as an incomplete practice or, in the case of mango, ineffective. The overall role of
pollinator diversity in influencing crop yields is continually being tested, demonstrating
the shift in strategic approach to pollination effectiveness and efficiency. The reliance
on insect pollination for agricultural crops is vital, with 39 out of the leading 57 single
crops seeing an increase in production with aid from these pollinators (Klein et al.,
2007). These crops make up 35% of global food production, demonstrating once again
the role of pollinator diversity in influencing crop yields.
Previous studies have suggested mangoes are anemophilous (wind pollinated)
plants (Kumar et al., 2016), however, Popenoe (1917) and Davenport (2009) brought
forth the idea that insects were responsible for the pollination of mangoes.
Hymenoptera and Diptera have been shown to be key orders of insect pollinators of
mangoes in various parts of the world. Apidae, Syrphidae, Tachinidae, and
77
Bombyliidae are just a few of the families containing species involved in mango
pollination (Larson et al., 2001).
Davenport (2009) indicated that self-pollination is a likely occurrence in flowers
while the pollen is still damp, and this self-pollination may be aided by insects moving
pollen between floral sexual organs. Others have also claimed that depending on the
cultivar self-pollination can occur (Dijkman & Soule, 1951). Despite these assertions, it
was established by Singh et al. (1962) that self-incompatibility occurs in monoembryonic
‘Dashehair’, ‘Langra’, ‘Chausa’, and ‘Bombay Green’ (Mukherjee et al., 1968; Sharma &
Singh, 1970) to name a few.
To provide evidence to support the importance of insects in mango pollination,
Popenoe (1917) conducted a bagging experiment to exclude insects and found that
when insects were excluded, it resulted in less fruit set. However, Wester (1920)
considered wind pollination a viable means of pollination in mangoes. Free and
Williams (1976) showed that bagged panicles still produced fruit set, suggesting the
transfer of mango pollen by wind occurred despite the fact that mangoes do not show
any physiological or morphological adaptations for wind pollination (Kumar, 2016).
Furthermore, mangoes have two types of flowers, hermaphroditic and staminate, both
with sticky-pollen, which may allow for pollen grains to adhere to insect structures
during nectar feeding, suggesting some type of insect interaction is necessary for
pollination (Usman et al., 2001, Huda et al., 2015; Willmer and Finlayson, 2014).
An increase in mango fruit set by cross pollination shown in previous studies is
evidence for arthropod pollination and indicates that despite potential self-pollination,
mango fruit set is often limited by pollen incompatibility and stigma deficiencies (Singh
78
et al., 1962, Huda et al., 2015). Although less than 50% of flowers receive pollen in
nature (Iyer & Schnell, 2009), augmenting insect pollinators could potentially alter this.
The stigma is most receptive within the first 6 hours of anthesis, but will remain viable
for 72 hours (Singh, 1960). Once pollen is received by the stigma, germination
transpires within 90 min (Singh, 1954). The physiology of pollination has been
documented (Sandip et al., 2015; Usman et al., 2001) in mangoes, however, how pollen
moves around and the role of insects in cross-pollination is still ongoing research.
To investigate the impact or benefit of insects in pollination of mangoes,
comparison studies similar to Popenoe (1917) and Free and Williams (1976) were
conducted in which inflorescences were bagged prior to anthesis restricting the
presence of insects. This is a common method often used to compare between a
positive and negative control in which the insect visitors are excluded for the entire
duration until fruit is present (Delaplane et al., 2013).
Material and Methods
The ‘Keitt’ mango orchard at the Tropical Research and Education Center
(TREC) was used to determine the importance of arthropods in fruit set. Twenty-two
trees were selected based on their availability of inflorescences that shared similarity in
panicle length and flower development (Figure 4-1). Eight inflorescences per tree were
selected for a total of 4 control and 4 bagged inflorescences. A total of 176
inflorescences were selected, 88 bagged and 88 controls that were spread throughout
the mango orchard at TREC.
Four arthropod excluding bags were placed on each tree over an inflorescence
that had not yet gone through anthesis. The mesh nylon bags were constructed of “No
Thrips” Insect Screen 75 Mesh, 134" Wide” from Greenhouse Megastore and were
79
sewn individually to measure 97 cm long and 116 cm wide (Figure 4-2). The screen
used for these bags allows the entry of air and light but excludes insects. Each bag
contains a drawstring located at the top to secure the bag around an inflorescence
rachis and a wire frame to limit contact between the screen and the flowers. The frame
was constructed of chicken wire that provided support of the mesh bags but was not too
heavy for the branches. A chicken wire structure (61 cm long and 64 cm wide) was
placed inside each bag. Galvanized utility wire was added around the base of the
branch to further secure the mesh bags around the inflorescence. The bottom of the
bag was left open for placement over the inflorescence while minimizing disturbance of
the flowers. The bottom of the bag was then tied to the limb around the base of the
inflorescence using zip ties. In some cases when the bag was too heavy, a string was
used to secure the branch to surrounding branches or the trunk, which provided
additional support to the branch (Figures 4-2, 3, 4). To exclude ants and other small
arthropods, tangle foot was applied at the base of each bagged inflorescence. Four
other inflorescences were tagged but not bagged for comparison. These inflorescences
were similar in size, maturity, and located near the bagged counterpart. Mesh bags
were placed on the trees over the course of a month during bloom and prior to fruit
development. Mesh bags remained in place during the entire bloom period until fruit
maturation when they were removed mid-July.
The number of fruit per bagged and control inflorescence was recorded and
compared from initial fruit set until mature fruit were present (Figure 4-5, 6, 7). Data
were collected twice between March 2nd and July 13th representing initial fruit set and
mature fruit set. A Welch Two Sample t-test was conducted to compare the relationship
80
between the fruit on bagged and control branches at both sampling points using
RStudio.
Results
Fruit set on the first sampling date was 6.7 times higher in inflorescences
exposed to insects compared to those where insects were excluded. Inflorescences
exposed to insects (un-bagged) averaged 2.69 ± 0.51 fruit per inflorescence which was
significantly greater than inflorescences where insects were excluded (bagged) which
averaged 0.4 ± 0.11 fruit per inflorescence (Figure 4-8) (t-value = -4.32, df = 181.78, P =
2.54e-05).
There was significant fruit drop between the first and the second sampling dates.
The number of fruit per inflorescence decreased 92% and 97% in un-bagged and
bagged inflorescences, respectively. However, the number of mature fruit on the second
sample date was 17 times higher in inflorescences exposed to insects as compared to
those where insects were excluded. There was an average of 0.17 ± 0.04 fruit per
inflorescence when exposed to insects (un-bagged) and 0.01 ± 0.01 fruit per
inflorescence when bagged as measured on the second sampling date when fruit were
mature (Figure 4-9) (t-value = -3.62, df = 97.62, P = 0.00047). Overall, the arthropod
exclusion tests revealed that insects can increase fruit set up to
Discussion
Arthropod exclusion tests suggest insects play an important role in the pollination
of mangoes and that wind pollination and/or self-pollination may be less of a factor than
previously noted. Free and Williams (1976) conducted a similar study in which mango
inflorescences that were bagged prior to anthesis to exclude insects did set fruit,
concluding pollen may also be transferred by wind. Although our findings do not entirely
81
refute this, as fruit set did occur in bagged inflorescences, our findings do reveal the
importance of arthropod interactions with mango flowers to improve fruit set.
There was a dramatic decrease in the amount of fruit set between the first and
second evaluation of March 2 and April 3, 2018. Fruitlet abscission in mangoes is
known to occur several weeks after anthesis resulting in a high percentage of panicles
to lose their fruit (Nunez-Elisea, 1986; Davenport, 2009). Different abiotic and biotic
factors may influence fruit set, including cold temperatures, high winds, low relative
humidity, limited nutrients, or lack of pollination. Research indicates that less than 1%
of fruit reaches maturity, which arises from the 8-13% of perfect flowers that set fruit
(Bijhouwer, 1937). Fruitlet abscission is random and may affect any fruit independent of
size or location on the panicle (Davenport, 2009). This suggests that in our study,
fruitlet abscission should be random, or that no pattern in mature fruit set between bag
vs. non-bagged treatments should exist if insects do not play a role in fruit set and
pollination. However, our results indicate arthropod involvement is important if not
essential to increased fruit set. Our data helps strengthen the importance of insect
involvement in mango pollination and provides more insights for future studies.
The sheer number of inflorescences on a mango tree coupled with naturally low
fruit set pose a challenge for investigating mango pollinators and their effect on fruit set.
Although 176 inflorescences were chosen, with 88 bagged and 88 non-bagged spread
across 22 trees, the low ratio of flowers to fruit set may limit a complete understanding
of how important insect pollination is for mango. It is also possible that bagged
inflorescences for prolonged periods may have limited some of the fruit present due to
factors other than insect exclusion. While the mesh bags were used to exclude
82
arthropods from mango pollination, these bags may also limit the amount of pollen
being transferred by wind. The idea of wind pollination has been previously postulated,
and thus the statistically significant difference between bagged and non-bagged may be
due to both reduced insect and wind pollination. Additional studies with more replication
may better indicate how important insect pollination is to mango fruit set and crop yields.
The absence of insects during anthesis lead to reduced fruit set. Given the low
percentage of fruit set as previously discussed, maximizing every tree in an orchard to
produce maximum fruit is important for efficiency, especially given the lack of land
available for planting more mango trees. Although our sample size of 176
inflorescences is relatively small, the difference in fruit production between bagged (1%)
and non-bagged (17%) was significant. In 2016, the U.S. Department of Agriculture’s
Economic Research Service (ERS), listed the average cost of a fresh mango at $1.32
and a dried mango at $10.16 per pound. Our results suggest insects are significantly
contributing to the profitability of mango production systems in Florida. Moreover,
management tactics targeted to improve pollination services could lead to a greater
income for farmers. For instance, implementation of native flowers in small clusters can
help increase pollination when complimented with other factors such as maintenance of
natural habitats that serve as pollinator reservoirs (Carvalheiro et al., 2012). Moreover,
environmentally friendly management approaches to reduce pesticide pressure and
increase insect populations may also improve pollination. Further studies aimed at
identifying effective tactics to preserve and augment mango pollinators in Florida could
increase the sustainability and profitability of mango production systems in Florida.
83
Figure 4-1. Pollinator exclusion bags (middle-right side) in the canopy of ‘Keitt’ mango
trees at the Tropical Research and Education Center, Homestead, Florida, on March 1, 2018. Photo courtesy of Matthew Quenaudon.
84
Figure 4-2. Pollination exclusion bag placed around a mango inflorescence prior to
anthesis on January 30, 2018. The panicle can be seen upright without any contact to the mesh nylon bag. Photo courtesy of Matthew Quenaudon.
85
Figure 4-3. A developing mango inflorescence on March 1, 2018, inside an exclusion
bag. Photo courtesy of Matthew Quenaudon.
86
Figure 4-4. A bagged panicle with no fruit-set or vegetative growth (March 15, 2018).
Photo courtesy of Matthew Quenaudon.
87
Figure 4-5. Initial fruit set on ‘Keitt’ mango. Fruit set varies throughout the panicle
(March 1, 2018). Photo courtesy of Matthew Quenaudon.
88
Figure 4-6. Fruit enlarging after initial fruit set (March 15, 2018). Photo courtesy of
Matthew Quenaudonon.
89
Figure 4-7. Fully developed fruit on July 28, 2018 at the Tropical Research Center,
Homestead, Florida. Photo courtesy of Matthew Quenaudon.
90
p = 2.54e^-05
91
Figure 4-8. The mean number (± SE) of fruit per panicle on non-bagged and bagged (insects excluded) mango
inflorescences on March 2, 2018, 50 days after bagging
92
p = 0.00047
93
Figure 4-9. The mean number (± SE) of fruit on non-bagged and bagged inflorescences on May 10, 2018, 140 days after bagging.
94
CHAPTER 5 CONCLUDING SUMMARY ON PRIMARY INSECTS INVOLVED IN MANGO
POLLINATION IN THE SOUTH-FLORIDA REGION
The notion that a good pollinator is subject to several criteria helps us process
which insects may be good candidates for mango pollination. Population density and
high frequency of insect to flower interactions are characteristics of the most effective
insect pollinators. Although pollination efficiency is a complex interaction influenced by
insect morphology, behavior, and flower characteristics, there is now a greater
understanding of the key insects visiting “Keitt” mangoes in south Florida. In addition to
insect population dynamics, understanding the ecological diversity and species
evenness as affected by time of day, location, and sampling period during bloom will
improve the identification and knowledge of the insects involved in pollination of
mangoes. Sampling throughout the entire blooming period provides a more reliable
representation of insects and life stages visiting mangoes in south Florida.
Primary insects included Musca domestica, Allograpta obliqua, Sarcophagidae,
and Camponotus plantatus that were all found to carry large amounts of pollen and
were prevalent throughout the mango orchards independent of location. In contrast, the
distribution and density of A. mellifera was significantly less than the Dipteran species.
This highlights the importance of Diptera in mango pollination and subsequently the
production of fruit. Our results indicated a large presence of flies within the first three
weeks of anthesis, critical time for pollination and early fruit set. Most of the insects
observed were Diptera and this may be the ideal time for augmentation of these
pollinators. Other potential pollinators included Brachiacantha baberi, Euphoria
sepulcralis, and Hippelates sp. Despite low numbers of B. baberi collected, this insect
was highly abundant in visual observations, suggesting further study.
95
Although A. mellifera contained the highest amount of pollen per insect, it’s lack
of visitation and seemingly disinterest in mango flowers limits it as a key pollinator. In
contrast, the density and prevalence of flies found to carry mango pollen is highly
significant. This suggests Hippelates sp., Liohippelates sp., Oscinella sp., Forcipomyia
genualis, Sciaridae, and Cryptophagus sp. may be important pollinators, however,
future research is needed to confirm this. Other insects that are potential pollinators
included Copestylum violaceum, Palpada mexicana, Ornidia obesa, Toxomerus
marginatus, and Lucilia coeruleiviridis. These five species of insects were not well
represented in our samples due to their speed and difficulty in collecting them with a
standard sweep net. Copestylum violaceum, Palpada mexicana, Ornidia obesa were all
observed to interact with mango flowers in the upper mango canopy (trees were up to
15ft tall). In addition to these insects there may be other pollinators that were outside
our sampling area.
In conclusion, this investigation identified the density, frequency, and behavior of
insects interacting with mango flowers during the 8-week bloom period of ‘Keitt’ mango
trees in three orchards in Homestead, Florida. Our results indicate that a wide diversity
of insects pollinate mango and there is a temporal shift of insects throughout the mango
bloom. When insects were excluded, there was an increase in fruit set up to 17%.
Moreover, differences in insect populations in separate orchards suggest that cultural
practices may have affected the populations of these insects and could be used to
increase these populations. Future research focusing on less observed and collected
insects such as C. violaceum, P. mexicana, O. obesa, and L. coeruleiviridis would help
to further fill the gaps in information of key pollinators for mango. Additional
96
investigations to increase pollination by augmenting mango orchards with the insects
shown in this research could be of practical and scientific value. Improvements of
cultural, biological, and physical methods to increase the natural populations of Musca
domestica, Allograpta obliqua, Sarcophagidae, Forcipomyia genualis, Hippelates sp.,
Liohippelates sp., Oscinella sp., Apis mellifera, and Camponotus plantatus may produce
an increase of pollination services in mango orchards.
97
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BIOGRAPHICAL SKETCH
Mr. Matthew R. Quenaudon finished his undergraduate degree of entomology at
Michigan State University in May of 2012. Matt went on to work as curator at The
Original Butterfly House & Insect World on Mackinac Island from May to Oct 2012. In
June of 2013, Matt worked as an integrated pest management intern at Phipps
Conservatory and Botanical Gardens, before working as integrated pest management
specialist in October 2013. Matt worked as an integrated pest management specialist
for 3 years until July 2016 before starting a master’s program at the University of Florida
in August of 2016. Matt is an entomologist with wide-ranging academic and
professional experience, who hopes to continue to translate his passion for nature with
a strong work ethic into a career grounded in positive ecological change. Matt strives to
use his expertise to tackle entomologic challenges both economic and environmental,
while challenging commonly-held stigmas about insects and emphasizing the
importance of insects to our world and way of living.