Provisioning Australian Seed Carrot Agroecosystems with Non-Floral Habitat Provides Oviposition Sites for Crop-Pollinating Diptera
The addition of floral resources is a common intervention to support the adult life stages of key crop pollinators. Fly (Diptera) crop pollinators, however, typically do not require floral resources in their immature life stages and are likely not supported by this management intervention. Here, we deployed portable pools filled with habitat (decaying plant materials, soil, water) in seed carrot agroecosystems with the intention of providing reproduction sites for beneficial syrphid (tribe Eristalini) fly pollinators. Within 12 to 21 days after the pools were deployed, we found that the habitat pools supported the oviposition and larval development of two species of eristaline syrphid flies, Eristalis tenax (Linnaeus, 1758) and Eristalinus punctulatus (Macquart, 1847). Each habitat pool contained an average (±S.E.) of 547 ± 117 eristaline fly eggs and 50 ± 17 eristaline fly larvae. Additionally, we found significantly more eggs were laid on decaying plant stems and carrot roots compared to other locations within the pool habitat (e.g., on decaying carrot umbels, leaves, etc.). These results suggest that deploying habitat pools in agroecosystems can be a successful management intervention that rapidly facilitates fly pollinator reproduction. This method can be used to support future studies to determine if the addition of habitat resources on intensively cultivated farms increases flower visitation and crop pollination success by flies.
Fly (Diptera) Pollination Efficiency and Reproductive Needs within Crop Agroecosystems
Global agricultural crop production has become increasingly pollinator-dependant. Eusocial bee taxa within the family Apidae (e.g., honey bees, bumble bees, stingless bees) are wellestablished, successful crop pollinators globally. In particular, the ubiquity and wellestablished management of the European honey bee (Apis mellifera Linnaeus, 1758) has resulted in an overreliance of this pollinator worldwide. As other non-bee insects are also effective pollinators, it has become increasingly important to better understand the capability and life history needs of non-bee pollinator taxa so they can provide alternative, or supplementary, pollination services to managed bees and be supported within the landscape. This will ensure that consistent and reliable pollination services continue to be supplied to agricultural systems. This thesis investigates the pollination effectiveness and reproductive needs of the second most important pollinator taxon behind bees, the flies (Diptera), in pollinator-dependant food crops.
First, I conducted a systematic literature review on the diets and habitat needs of 431 crop flower-visiting fly species found globally and collated the existing information into a database. I was able to document the diets and habitat needs of 242 crop-visiting fly species (24 families and 119 genera) inhabiting all eight global biogeographical regions. I found that these crop-visiting fly species live in 35 different natural habitats and belong to 10 different feeding guilds. The results of this review identified major gaps in our understanding of the life history needs of crop-pollinating flies. In particular, current floral management schemes are largely focused on the resource needs of bees. As flies require other non-floral habitats to complete their life cycles, the diverse life history needs of flies and other non-bee taxa are not currently supported by existing pollinator management practices.
Second, I investigated the identity and efficiency of floral visitors to carrot seed crops. To do this, I conducted floral field surveys and pollen deposition trials across two years (2020-21) within varying environmental conditions in the Riverina region of New South Wales (NSW). I conducted 268 floral visitation surveys and identified 53 different insects (26 families) as floral visitors of seed carrot in temperatures ranging from 10.5ºC to 39.5 ºC and in 19.7% to 94.7% relative humidity. Spatial and temporal complementarity was observed across all dominant taxonomic groups (ladybeetles, bees, flies). Wild taxa generally matched managed honey bees in terms of abundance and their capability to transfer pollen between carrot parent lines. Further, wild taxa, not managed European honey bees deployed for pollination services, are providing the bulk of pollination services to Australian hybrid seed carrot.
Third, I determined the oviposition and habitat needs of pollinating hoverflies (Syrphidae: Eristalini). I did this by deploying 14 portable pools filled with soil and decaying vegetation across four seed carrot sites in the Riverina (NSW) region of Australia. All pools successfully supported the immature stages (eggs and larvae) of hoverflies after 12 to 21 days, and two beneficial species of flies were reared from the pools: Eristalinus punctulatus and Eristalis tenax (Linnaeus, 1758). Both species were effective pollinators of seed carrot in Chapters Three and Four of this thesis, respectively. These results suggest that deploying portable habitat pools filled with decaying plant materials in agroecosystems may be a successful management intervention to rapidly facilitate hoverfly pollinator reproduction.
Fourth, I assessed the effectiveness of the Australasian endemic golden native dronefly Eristalinus punctulatus (Macquart, 1847), at transferring pollen to hybrid seed carrot flowers. While both honey bees and the native drone fly were capable of depositing pollen onto seed carrot floral stigmas, golden native drone flies on average deposited more pollen onto stigmas than European honeybees. I also observed the first recorded event of natural oviposition of this fly species on the Mid North Coast (NSW) region. When observing the oviposition of this fly, I found that they oviposited within discarded raspberry plant root balls at a commercial berry farm. This observation, coupled with their demonstrated pollination effectiveness in seed carrot, suggests that these endemic flies could be supported as potential pollinators by deploying non-floral habitat within agroecosystems.
Finally, I compared the pollination effectiveness and activity patterns of two managed fly pollinators and two managed bee species at commercial raspberry and blackberry farms in two major berry growing regions in Australia: Mid North Coast (NSW) and Northern Tasmania (TAS). All taxa were capable of effectively pollinating raspberry and blackberry after one visit to a flower; however, the quality, weight, and number of pollinated drupelets per fruit varied depending on the taxa tested. In small cages, E. tenax and wild taxa pollinated raspberry fruits that weighed significantly more and were of higher quality than fruits harvested from C. stygia cages; however, there were no significant differences in the quality, weight, and number of pollinated drupelets in blackberry across all taxa. Further, in a blackberry polytunnel in Tasmania, E. tenax flies were significantly more active than European honey bees, and the fruits harvested from the E. tenax polytunnel did not differ from fruits visited by honey bees. These results demonstrate that some fly species could be effective supplementary, or alternative, pollinators to managed bees in commercial raspberry and blackberry.
This thesis demonstrates the importance of understanding how wild taxa, like flies and non-Apis bees, contribute to pollination service delivery, and how best to support these taxa within agroecosystems. Some flies and other wild taxa can provide significant and effective pollination services to some crops. If supported with foraging and habitat needs, these taxa may be able to provide similar pollination services to the honey bees used within these systems. Identifying wild pollinator taxa and their life history needs, assessing their capability as pollinators in a variety of crop systems, developing rearing techniques to commercialize effective taxa, and methods to support effective wild and managed pollinator assemblages within agroecosystems, are all important next steps to improve pollination services and yields of pollinator-dependant cropping systems globally.
Fly (Diptera) pollination efficiency and reproductive needs within crop agroecosystems - Dataset
This dataset consists of eight tabs (the first four relating to Chapter 2 and the remaining four relating to Chapters 3, 4, 5, and 6 of my thesis). All data related to this thesis was collected online from the Web of Science and Scopus search engines (Chapter 2), the CropPol and Rader et al. 2020 public databases, and in the field from Griffith, New South Wales, Australia (Chapters 3, 4, and 5), from the East-North Coast of New South Wales, Australia (Chapter 6), and from Northern Tasmania, Australia (Chapter 6). Each tab has an excel spreadsheet with data from each thesis research chapter, and the content of each tab is explained below: Chapter 2.1: A review of the life history needs of the larval and adult stages of crop flower-visiting flies (Diptera). This dataset consists of family, genus, and species names extracted from public pollination databases ('CropPol' or 'Rader et al. 2020'), the total number of searches the species name received from Scopus and/or WOS (Web of Science), whether the information for the diet and habitat needs were found ('Accessible' or 'Inaccessible'), the total number of larval and adult feeding guilds the fly may utilize ('Unknown', 'One', 'Two', 'Three', 'Four', 'Five', or 'Six'), whether the fly utilizes the same feeding guilds in both active developmental stages of life ('Unknown', 'Different', or 'Same'), and finally the dataset in which the species name was extracted from ('CropPol' or 'Rader et al. 2020'). Chapter 2.2: A review of the life history needs of the larval and adult stages of crop flower-visiting flies (Diptera). This dataset consists of adult fly life history information extracted from reviewed articles, such as the feeding mechanism (e.g., chewing decaying animal flesh, sucking blood, etc.), habitat, and feeding substrate of specific crop flower-visiting fly species. The quality of this extracted information is placed in two categories ('Validated in experiment', or 'Inferred (by authors)'). Chapter 2.3: A review of the life history needs of the larval and adult stages of crop flower-visiting flies (Diptera). This dataset consists of the larval fly life history information extracted from reviewed articles, including the feeding mechanism (e.g., chewing decaying animal flesh, sucking blood, etc.), habitat, and feeding substrate of specific crop flower-visiting fly species. The quality of this extracted information is placed in four categories ('Validated in experiment', 'Inferred (by authors)', '(Validated by) Expert', and 'Unable to access'). Chapter 2.4: A review of the life history needs of the larval and adult stages of crop flower-visiting flies (Diptera). This dataset consists of the data on the biogeographic host range of the species and was extracted from species catalogues, manuals, and websites (‘References’) managed by experts in the field of Dipterology. One species may occupy more than one biogeographical region. Chapter 3: Floral visitation surveys of insect visitors of hybrid seed carrot (Daucus carota subsp. sativus) crop plants. Surveys were conducted up to three times a week during full bloom (22 November to 5 December 2021) at six sites throughout the day (05:00 to 17:00). Surveys were conducted along two, 10 m transects: one along the edge of the carrot field and an additional walk in the middle (> 30 m into the field). All transects were conducted walking slowly (1 m per minute when possible) between two rows of carrot plants (either ‘Male’ and ‘Female’ or ‘Monoecious’ and ‘Monecious’). The temperature and relative humidity was recorded using Kestrel® Drop D2 data loggers permanently deployed in a shaded location within, or nearby, all study sites. All insects were identified to the lowest taxonomic level using dichotomous keys. Chapter 4: Deploying habitat to support the immature life stages of eristaline flies (Syrphidae) in hybrid seed carrot crop agroecosystems. In a paired experimental design, two habitat pools filled with substrates (‘carrot’ and ‘soil’) intended to attract eristaline flies were deployed at 7 sites. The pools were placed between 15 November to 24 November 2021 and left to decay for 12 to 21 days. Surveys of the immature life stages (‘eggs’ and/or ‘larvae’) were identified and counted within the pools. The state of the larvae (‘first instar’, ‘second instar’, ‘third instar’, or ‘dead’) as well as the location where batches of eggs were laid within the deployed habitat were determined. Chapter 5: Effectiveness of fly and bee pollinators at pollinating hybrid carrot plants grown for seed. This dataset consists of stigmas collected after a single visit by one pollinator species. The first column is date the replicate was collected, the second column is the pollinator species, the third column is the duration of time in seconds the pollinator spent visiting the replicate, the fourth column is the number of stigmas mounted on the slide, the fifth column is the number of pollinated stigmas (at least one pollen grain touching the stigma), and the sixth column is the total number of pollen grains touching the carrot stigmas. Chapter 6: Efficiency of fly and bee pollinators at pollinating blackberry (Rubus fruticosus) and raspberry (Rubus ideaus) crop plants. This dataset consists of berries harvested after single visitation (one visit to a flower), unlimited visitation (allowed access to flowers in a small cage setting), and open pollination (scale of a farm polytunnel) treatments under field conditions. The first column is the unique pollinator ID, the second column is the pollinator species, the third column is the type of trial (‘Cage’ or ‘Field’), the fourth column is the weight of the harvested fruits, the fifth column is the number of drupelets per fruit, the sixth column is type of defect found in the fruit (’None’, ‘Progressive’, or ‘ Critical’) as per industry standards, and the seventh column explains the type of defect seen in the fruit (if any).
The golden native drone fly (Eristalinus punctulatus) is an effective hybrid carrot pollinator that lives within Australian crop agroecosystems
1. Native insect flower visitors can be important contributors to crop pollination, yet little is known of their pollination abilities and the resources (habitat) they need to be supported within crop agroecosystems.
2. Here, we compared the abundance and pollination abilities of the golden drone fly (Eristalinus punctulatus) to the European honey bee (Apis mellifera) in hybrid carrot crop fields known to produce variable seed yields in regional New South Wales, Australia. We further observed the egg-laying behaviours of female golden drone flies at a commercial berry orchard to provide insight into the habitat needs of this species.
3. In hybrid carrot crop fields, golden drone flies were far less abundant flower visitors than European honey bees" however, these flies deposited more carrot pollen grains on average (8.21±3.04SE) onto carrot flowers than European honey bees (3.45±1.06SE). Both insects also deposited pollen onto a similar number of carrot flowers (pollinated) per visit (about 2 out of 18).
4. Golden drone flies were observed laying eggs within masses of discarded red raspberry plant roots and soil (root balls) at a commercial berry orchard. The natural habitat utilised by these flies, as well as their egg-laying behaviours, were described for the first time.
5. Our results indicate that golden drone flies are effective pollinators of hybrid carrot crop plants. The habitat that these flies utilised to lay eggs (discarded plants and water) is cheap and commonly found in crop agroecosystems. Therefore, we recommend placing this low-cost habitat within, or nearby, crop fields as a potential management practice to support the lifecycle needs of golden drone flies and other non-bee pollinators.