Eucera longicornis at Gatwick airport is an example of how human intervention and land management can aid wildlife conservation of a rare and endangered species. The two nest aggregations are both in man-made habitats and appear to have stable female populations of reasonable size, so far as this 3-year study can reveal. Aggregation 1, the larger, had estimated female populations of over 400 in 2019 and 380 in 2018, versus 146 and 183 for aggregation 2. Fabaceae species were the main pollen sources for E. longicornis, averaging 95% of samples. Within 100 m of the nest aggregations these Fabaceae species were abundant and many were also growing in man-made or altered habitats.
Estimates appear to indicate that the populations were approximately stable between 2018 and 2019 with both populations smaller in 2017. However, surveys in 2017 were for a much shorter period and did not include male estimates due to starting after the period of male activity. Males emerged before females, with peak population estimates either in late May or early June, compared to middle to late June for females. Earlier emergence of males is common in solitary bees and other insects (Wiklund and Fagerström 1977) and is generally due to mating strategy, with males waiting to mate with newly emerged females.
Both aggregations had female biased sex ratios in 2019, (aggregation 1, 2019 1:3.4; aggregation 2, 2019 1:4.3). In solitary bees, sex ratios have been found to deviate from the predicted Fisherian 1:1 ratio (Rosenheim et al. 1996). These deviations are often due to differences in parental investment for each sex as well as local mate competition and limited egg production (Herre 1985; Rosenheim et al. 1996). Sexual dimorphism is common in Hymenoptera, generally with females being larger (Helms 1994). This is true for E. longicornis, with males on average weighing 0.048 g compared to a female average of 0.066 g (Saunders pers. comms.). This results in an expected male bias sex ratio in the population, as males should be less costly to produce. However, when local resource availability is good this can result in investment in the more costly sex to be advantageous (Kim 1999). This is because females can allocate more resources to each individual offspring (Peterson et al. 2006). Perhaps the increase of both female populations indicates favourable foraging conditions in the areas surrounding the aggregations.
We are unsure as to why the aggregations in this study have such a high female sex bias, and why this bias was not present in aggregation 1 in 2018. Although local mate competition and inbreeding can cause female bias (Herre 1985), this seems unlikely to be the case with E. longicornis, as mating occurs outside the natal nest and males are seen searching for mates at the nest sites. From a conservation perspective, female bias may be advantageous. The males present would be sufficient to fertilise the females and the larger number of females would boost the number of brood reared, with the effect on effective population size being small (Wright 1993).
In the Hymenoptera the risk with a highly skewed sex ratio in a population is the reduction of the equilibrium number of sex-alleles. However, the population size estimated for E. longicornis at Gatwick appear to be greater (> 100) than would give cause for concern in terms of sex alleles and diploid male production in a species with complementary sex determination (Zayed 2004).
It is possible that the biased sex ratio is due to the methods used, with females perhaps easier to capture than males. However, capture probabilities for males were estimated to be higher than for females in 2019. Survival estimates for males in 2019 at both aggregations were lower than in 2018 and lower than the female estimates, with a large reduction in survival for males in aggregation 1 between years (2018;0.93, 2019;0.36). We are unsure as to why the estimated survival rate for males was so much lower in 2019 for aggregation 1. The difference in survival between males and females may be due to males not having a nest to return to either at night or during times of bad weather (Alves-dos-Santos et al. 2009). Males also often disperse from the natal nest site (López-Uribe et al. 2015) and if not caught before this time would not be included in the population estimate. Higher mortality or dispersal rate of males could partially explain the female bias sex ratio seen in these populations.
By placing emergence traps and digging up nests and examining cells the true sex and investment ratios could be determined.
Nest site characteristics
Eucera longicornis tends to nest on south facing, soft banks of bare soil or cliff face in the locations where it is found (Saunders 2014). In agreement with this, both Gatwick aggregations are nesting in sloped banks. Both these nesting sites exist as a result of human intervention. At Gatwick Airport, aggregation 1 is nesting on a manmade raised mound of excavated soil, and aggregation 2 along the bank of the river Mole (Fig. 3). In 1999 Gatwick Airport diverted a section of the river to allow the expansion of the airport’s western boundary. A new channel to the west of the old course, plus the shortening of a connecting western tributary, resulted in the river being moved a few hundred meters to the west of the original course. This new channel was altered to meander and allowed the creation of new habitats, such as the meadow along the length of the channel (British Airport Authority 2004). Through the altering of the river, the bank with aggregation 2 was created. Some of the soil excavated during the project was left on Gatwick land to eventually become the heap in which aggregation 1 is located. It is unlikely that E. longicornis were present before this land management. This an example of how an industrial/commercial area, such as an airport, can manage the surrounding landscape in such a way as to create habitats and thereby help the conservation of a nationally rare species of wildlife.
Both nest aggregation sites have little vegetation cover and many patches of bare ground, a common characteristic of ground nesting bees (Wuellner 1999; Sardinas and Kremen 2014). Aggregation 1 has not moved from or expanded its nest location since it was first identified in 2014 (Rachel Bicker Pers comms). As of 2018, aggregation 2 has extended 20 m further along the bank from its original location.
Surveys conducted along the banks of the river Mole and along suitable banks near aggregation 1 as part of this project as well as surveys by the Gatwick biodiversity team, have not discovered additional nest aggregations. Many species of solitary bees exhibit nest philopatry (Yanega 1990; Potts and Willmer 1997) in which newly- emerged females nest at their natal nesting site, instead of leaving to nest elsewhere. This will often have selective value for a foundress, as the natal nest site was successful enough to produce adults in the previous year, and therefore, is likely to be suitable again (Potts and Willmer 1997).
Limited availability of nest sites is also a reason why females may nest in their natal area instead of finding a new site (Batra 1978). However, at Gatwick there appear to be many banks of soft, bare soil, like the ones which already contain aggregations close by at both aggregations (< 10 m). If the female population continues to grow and nest density capacity is reached, dispersal from these aggregations is possible with new aggregations potentially being formed beyond the area surveyed. A male E. longicornis was sighted approximately 1 km from aggregation 2 (Pers comms. Laurie Wright). This male may be from one of the aggregations in this study, or potentially a new aggregation not identified. Future surveys covering a wider area are required.
Pollen collected from returning females from both aggregations was predominantly Fabaceae species which was present in all (113) samples taken from individual females and always accounted for more than 90% of the total grains in a sample. Pollen was identified as Trifolium, Lotus, Lathyrus and Vicia species. The most common non Fabaceae species was bramble, R. fruticosus which averaged 5%. This narrow familial range of pollen collection indicates that E. longicornis is oligolectic (Mueller and Kuhlmann 2008) and agrees with previous research (Saunders 2014). Visual sightings of males on Symphytum orientale (white comfrey), a species of pollen not identified in female pollen loads, indicates a slightly broader foraging range than for female pollen collection. Differences in male and female foraging preferences are often seen in solitary bee species (Ritchie et al 2016) even in those with a narrow diet breadth. This is most likely due to males not needing to collect pollen for cell provisioning. In addition, male solitary bees normally emerge earlier than females, as seen in this study, so that the floral composition in the area will be slightly different, influencing what species they forage on.
Fabaceae pollen sources were most abundant in the meadow habitats (Fig S3, Supplementary Materials) for both aggregations, and within 100 m of aggregation 1 meadow is the predominant habitat type (72%). The proximity of the appropriate floral resources to the nesting sites is important as E. longicornis is reported to have a foraging range of approximately 500 m (Saunders 2014). An abundance of good quality forage near to the nesting site helps reduce the costs of foraging and therefore potentially increases reproductive output (Zurbuchen et al. 2010a, b).
E. longicornis conservation status
Eucera longicornis is in decline in Britain and other parts of its range (Pekkarinen 1997; BWARS 2012). In Cornwall, a stronghold for the species, there has been a 55% reduction since 1987 in the number of sites where it is found, from 24 to 11 (Saunders 2014). This is thought to be due to a combination of the loss of flowering legumes, increased extreme storm events along their coastal sites destroying nests, and a lack of sites containing both early and late flowering legume species such as Anthyllis vulneraria and Lathyrus sylvestris (Saunders 2017). Fabaceae species often occur in flower rich grasslands, which are declining in the UK (Goulson et al. 2005). This is due to a variety of factors, predominantly changes in agricultural practices. Between early and late twentieth century, fodder crops declined by more than 55% and were replaced with permanent grassland (Ollerton et al. 2014). These changes in landscape management have resulted in both a reduction in the range of many of the pollen sources E. longicornis rely on, as well as their frequency at a more local scale. For example, L. pratensis, a major pollen source for E. longicornis, reduced in frequency by 45% in the UK between 1978 and 1998 (Carvell et al. 2006). Owing to airports often having semi-natural grasslands surrounding runways, they have the potential to provide this much declining habitat which contains the floral resources that E. longicornis and other species need.
Management plans and future research
Although not known for their wildlife value or biodiversity, if managed correctly airports can provide a refuge for some species, as seen with E. longicornis at Gatwick. Another example is the presence of rare ground nesting birds at John F. Kennedy (JFK) airport in New York City, USA. The upland sand piper, grasshopper sparrow, and horned lark have all been found nesting in the airports semi-natural grassland habitat (Chevalier and Cohen 1997; Kershner and Bollinger 1996). A high abundance and diversity of arthropod species have also been identified at JFK (Kutschbach-Brohl et al. 2010), highlighting that if managed correctly airports have the potential to benefit wildlife.
There are over 60 major airports in the UK (Civil Aviation Authority 2020) and with the growing demand for airline travel the size and demand on airports is likely to increase (Upham et al. 2003). This highlights the importance of surveying airport land for wildlife and ensuring the land is managed effectively. Currently, Gatwick Airport’s management of the study area involves a single September cut of the meadow around the two aggregations, and coppicing of the woodland to help create and maintain compartments for wildflowers (Rachel Bicker Pers comms.), which should be continued. Ensuring the woodland surrounding the aggregations does not begin to encroach on the meadowland is also essential (Table 4).
Continued monitoring of the aggregations is recommended and, hopefully, to confirm that the existing management is effective. The mark recapture method used in this study is highly intensive and therefore, is likely to be impractical for future monitoring of population sizes unless additional staff are recruited. However, the population can be monitored in other ways. Counts along transect routes, recording number of nest holes at each aggregation site, and fixed standardised counts of activity at the aggregations are all potential population monitoring methods. For further information on management and monitoring suggestions see Table 4. These latter methods require less training but can still give a quantitative measure of population size (Bischoff 2003; Larsson and Franzen 2008) that could be compared across years to quantify any trends or changes. From what we can see from the current management and situation, it appears the two aggregations at Gatwick Airport are not threatened. Both have additional unused nesting space nearby and abundant forage and both foraging and nesting location are not in danger of becoming unsuitable either from natural or human factors.
Future work on these aggregations could consist of surveys of the surrounding soil banks, which are currently not being used as nesting sites, to determine if new nesting aggregations are founded. E. longicornis is also a key candidate for citizen science due to the males distinctive and unusual appearance, with their long antennae unlike any other native bees to the UK. This would make is possible to carry out a large-scale survey of the surrounding area using information from local residents. In 2018 a male was recorded approximately 3 km South East of the existing aggregations (NBN atlas 2018), perhaps indicating more nesting sites in the local area.
In many cases human changes to the landscape are detrimental to species and biodiversity (Winfree et al. 2011; Senapathi et al. 2015). However, through effective management biodiversity can be maintained and some species can even thrive in these human-altered landscapes (Macadam and Bairner 2012; Sirohi et al. 2015). Although E. longicornis is in decline throughout its range, by monitoring and conserving small populations like those at Gatwick, the conservation of this charismatic species may be possible.