Summary of the diet profiles
In this study, the dietary composition of House Swifts in Hong Kong was analysed using DNA barcoding to identify prey items in faecal samples. Hymenoptera, Hemiptera, Diptera, Blattodea, and Coleoptera were identified as the major prey groups of House Swifts in this study. The major prey groups identified in faecal samples were similar to those identified in stomach contents in previous studies of the House Swift diet (Kow 1980; Nguyên Quang et al. 2006). Cucco et al. (1993) reported that Hymenoptera, Hemiptera, Diptera, and Coleoptera were the four most common groups of prey for aerial-feeding birds and there was no exception found in this study. Moths, butterflies, and dragonflies have also been found as prey items for House Swifts. Kow (1980) and Nguyên Quang et al. (2006) also identified Lepidoptera and Odonata as prey items in their dietary studies, but, similar to the findings presented here, they were found to be relatively minor prey items.
Hymenopterans were found to be predominant in the diet of House Swifts during the breeding season, and ants (Formicidae) were the most prevalent members of this group. The previous two studies of the House Swift diet also reported a greater prevalence of Hymenopteran prey, especially ants, during breeding seasons (Kow 1980; Nguyên Quang et al. 2006). Ant alates, which perform nuptial flights for reproduction, are found in dense aggregations in the air and the exploitation of swarming insects by swifts has been reported frequently (Lack and Owen 1955; Hespenheide 1975; Marín 1999).
Hespenheide (1975) suggested that ants were relatively weak fliers when compared to more agile groups of insects, such as Dipterans, and thus, swifts may prefer preying on swarming ants rather than other aerial insects present in the air column. This may, in turn, reduce the capture effort and energy expenditure required by House Swifts. The reduction of capture effort is an important factor contributing to reproductive success, according to the optimal foraging theory (MacArthur and Pianka 1966). However, further research is necessary to determine the preferential foraging behaviour of House Swifts, as there are no data currently available regarding the presence and relative abundance of different kinds of aeroplankton species in Hong Kong.
In addition, some of the genera and/or species found in this study did not have previously known record in Hong Kong when compared to local insect checklist (Lau 2019; Table 2). For instance, Passeromyia, an underrepresented fly genus, with larvae known to be parasitic to bird nestlings (Grzywacz et al. 2014), was identified in the diet of House Swift. However, serious prudence should be taken when interpreting the unrecorded species, especially without morphological supports.
Presence of insect pests in the diet
Coleopteran prey items were found at a greater proportion in the diets of House Swifts in previous studies when compared to their dietary proportion in this study. Kow (1980) found that over 40% of the total stomach content was made up of Coleopteran prey, with a frequency of occurrence greater than 80%. Coleoptera comprised 17% of the total prey content, with a frequency of occurrence greater than 60% in the study performed by Nguyên Quang et al. (2006).
In fact, 70% of the Coleopteran prey found in Kow’s study were notorious grain pests, including the Cadelle Beetle (Tenebroides mauritanicus), Red Flour Beetle (Tribolium castaneum), and Lesser Grain Borer (Rhyzopertha dominica). The Rice Weevil (Sitophilus oryzae) contributed a further 7% within this prey group (Kow 1980). The exploitation of cereal farmlands by Coleopteran pests may be the reason for the large proportion of prey items found to be Coleopteran pests in the study in Yunnan. In Hong Kong, agricultural activities are restricted to a small scale and most agricultural land is used to grow gardening crops and vegetables to satisfy local demand (Agriculture, Fisheries and Conservation Department HKSAR 2019). Therefore, grain-associated Coleopteran pests are not likely to be as abundant in Hong Kong, as they are in other localities with more extensive cereal farming.
Kow (1980) found that greater than 80% of the prey items identified in the stomachs of House Swifts could be categorised as economically important or disease-spreading pests. Similarly, a high proportion of pests were found in the diet of House Swifts in Hong Kong, with 20 out of the 44 identified families consisting of members that are economically important pests or vectors of insect-borne diseases (Table 2). These pests were found to have %C and %FO values of 65% for all samples. Kow (1980) estimated that each House Swift can consume more than 1 kg of aerial insects each year, which indicates a possible role of House Swifts in reducing the number of local pests.
For instance, the Striped Flea Beetle, Phyllotreta striolata, a common agricultural pest that consumes cruciferous crops, like Chinese flowering cabbage in local farmland (Agriculture, Fisheries and Conservation Department HKSAR 2005), was identified in the diet at a significant proportion within the Coleopteran group. The Brown Planthopper (Nilaparvata lugens) and White-backed Planthopper (Sogatella furcifera), which are infamous rice pests that cause major paddy rice yield losses each year in East and Southeast Asian countries (Hu et al. 2017), were also identified in the diet, along with other agricultural pests, including the Rice Root Aphid (Rhopalosiphum rufiabdominale), Stem Borer (Sesamia inferens), and Maize Weevil (Sitophilus zeamais).
Haematophagic mosquitoes (Culicidae) were also a component of the House Swift diet and Culex spp. were found to make up a large proportion of the diet in winter. Some of the local Culex spp. are known to transmit Japanese encephalitis to humans (Zhao et al. 2018), but the species identified in the House Swift diet have not yet been confirmed as zoonotic vectors. It is worth mentioning that House Swifts almost exclusively prey on a single species of mosquitoes, Culex vagans, and this species was found in samples from all the study sites. The reason for the prevalence and widespread preference of a single species is unknown, but Culex spp. are known to feed on the blood of avian hosts and Culex pipiens has been shown to preferentially select a specific avian host (Simpson et al. 2009). Thus, a possible scenario is that Culex vagans preferentially fed on swifts, while also being consumed by the swifts. Further investigation is required to confirm such a complex parasite-host interaction.
The diet also consisted of the Red Imported Fire Ant (Solenopsis Invicta), which is a notorious invasive species first discovered in Hong Kong in late 2004. These ants cause damage to economically important crops worldwide and their stings can cause fiery sensations or even induce strong immune responses (Wong and Yuen 2005). The presence of the Red Imported Fire Ant in the diet of local House Swifts implies that nuptial flights may be the route used for their rapid spread and colonisation in Hong Kong.
Seasonal and site differences in diet profiles
Seasonal differences in dietary composition were found in this study, with Hymenoptera being most prevalent in the breeding season, but Diptera and Hemiptera showing the greatest prevalence in the non-breeding season. The seasonality shown in this study was similar to the results of a forest invertebrate seasonal study performed by Kwok and Corlett (2002) in Hong Kong, in which Malaise traps were used to capture flying insects in the understory of the Tai Po Kau Nature Reserve, a secondary forest near the CUHK nest sites used in this study. They found a high abundance of Hymenoptera in summer and a low abundance in winter, coinciding the changes in the abundance of Hymenopteran preys between breeding and non-breeding season of the House Swifts in this study.
Further, they found that Diptera was the most frequently captured insect group. However, these insects did not follow a seasonal pattern and were found at high abundance and biomass levels, even in winter when all other groups of insects captured showed relatively low biomass levels. This observation was also in line with the higher prevalence of Dipteran prey items observed in the diet during the non-breeding season in this study when the availability of Hymenopteran preys was low. Hemiptera species were also found to be the predominant prey items for house swifts during the non-breeding season, especially for the CUHK colony. However, the Malaise trap study lacked data on Hemiptera and Homoptera abundance in any season and thus, a comparison cannot be made for these groups.
It is clear that the presence of aerial arthropods shapes the diet of any opportunistic aerial feeder. Hence, seasonal variation in the composition of the local arthropod community contributes to the changes in the dietary composition of House Swifts between seasons.
This study also found no significant differences in dietary composition between different colonial sites within Hong Kong. Chan et al. (2019) showed that landscapes within the home range of swiftlets affected the composition of the diet. Although no tracking study has been performed for House Swifts, the average home range of the edible-nest swiftlets, Aerodramus fuciphagus, has been shown to be approximately 64 km2, with a flying distance ranging from 2 to 6 km (Burhanuddin and Noor 2017).
If House Swifts have similar home range, swifts from the five studied sites would cover similar mixed landscapes, comprising of urban and suburban areas, in which most of the nest sites were situated; as well as Country Parks, which are mostly secondary woodlands or shrublands (Delang and Hang 2009). Thus, the similar landscapes within the home ranges of the different nest sites may explain the similar dietary compositions found at the different sites in this study.
Efficacy of molecular profiling of bird diet
Of all taxa recovered in this study, 60% and 40% could be identified to the species and genus level, respectively. However, compared to dietary studies of insectivorous bats using faecal samples for DNA barcoding, the identification rate was relatively low. For example, in a study of the diets of multiple bat species in England, 72% of the sequences showed over 99.3% similarity with reference sequences deposited in the BOLD system and the majority were identified to the species level (Zeale et al. 2011). In a study of Little Brown Bats (Myotis lucifugus) in Canada, the majority of sequences were identified to the genus or species level after comparisons to reference sequences in the BOLD system (Clare et al. 2011).
The absence of reference barcodes in the database that match the query sequences is the main factor that hinders species-level identification. Less effort has been put into the deposition of insect barcodes in the reference database in Asian countries, which may explain the relatively low identification rate in this study compared to studies conducted in Europe and North America. A recent study of swiftlet diets using DNA barcoding, conducted in Malaysia, also had difficulties in successful identification up to low-ranked taxa. Out of 266 operational taxonomic units with prey sequences identified from swiftlet faecal samples, only three were successfully identified to the species level (Chan et al. 2019). Despite the identification to precise taxa being one of the major advantages of DNA barcoding over conventional dietary analysis methods, incomplete barcode databases greatly limit the potential of DNA barcoding for precise dietary analysis. Thus, joint efforts between Asian countries in the deposition of local or regional arthropod barcodes into the barcode database would be beneficial for future studies.
Moreover, despite the fact that many dietary studies based on DNA barcoding have attempted to use clone proportion or relative read abundance as estimations of the actual proportion of prey intake by the predator, these methods are controversial, as mismatches between the universal primers and the template can cause major bias in the proportioning of prey DNA, making quantitative data less reliable. This problem has been demonstrated in mock testing (Piñol et al. 2015).
Clone proportion was calculated in this study, but this metric should not be interpreted as the actual abundance in House Swifts’ prey, but rather treated as auxiliary to the frequency of occurrence. Qualitative dietary metrics are more reliable indicators of the actual dietary composition of House Swifts in this study, but they have the risk of overrepresenting rare prey items that have low abundance in each sample, but are prevalent in a set of samples (Deagle et al. 2019). However, since the %C and %FO values were similar, %FO may be a reliable indicator of the contribution of different prey groups in this study.
The non-asymptotic taxon accumulation curves also suggested that prey taxon discovered in this study might under-represent the actual diet of the House Swift in Hong Kong. Environmental degradation of DNA in faecal samples is one of the major obstacles in recovering prey. It has been demonstrated that exposing samples to sunlight and rain can greatly prey DNA amplification (Oehm et al. 2011).