Introduction
Ground cover plants at airports form an ecological community with special functions and roles. They play an important role in ensuring the safe takeoff and landing of airplanes and have the potential to provide habitat for insects living in, feeding in, and moving through the area (Soldatini et al., Reference Soldatini, Georgalas, Torricelli and Albores-Barajas2010). Aircraft−wildlife strikes (mostly by birds, referred to as birdstrikes) occur frequently throughout the world and pose a major hazard to flight safety, resulting in the damage of aircraft and the loss of life (Servoss et al., Reference Servoss, Engeman, Fairaizl, Cummings and Groninger2000; Soldatini et al., Reference Soldatini, Albores-Barajas, Lovato, Andreon, Torricelli, Montemaggiori, Corsa and Georgalas2011; Allan et al., Reference Allan, Baxter and Callaby2016). In general, insects are regarded as an attractant for birds, which are a known hazard in aviation (Hauptfleisch and Dalton, Reference Hauptfleisch and Dalton2015; House et al., Reference House, Ring, Hill and Shaw2020). Insects, as an important component of the ground cover community, form a stable food network together with vegetation and birds, and the species composition and abundance of insects are closely related to the composition and abundance of birds (Cardoso et al., Reference Cardoso, Gomes, Santos, Tavares and Guzzi2014; Li et al., Reference Li, Li, Nie, Jiang and Zhao2017).
There have been many studies on the insect communities within the different habitats of airport grasslands; however, information regarding the effects of artificial control measures on insect communities at airports is limited. Wang et al. (Reference Wang, Hu, Liao and Yu2013) investigated the insect community in seven different grassland habitats at Kunming Wujiaba International Airport and found that insect species richness was highest in the dandelion community and lowest in the Sporobolus fertilis community. Zhao et al. (Reference Zhao, Tang, Wang, Fan, Zhao and Yang2004) proposed that the diversity of grassland vegetation in the flight areas might enhance the diversity and abundance of herbivorous insects. Kutschbach-Brohl et al. (Reference Kutschbach-Brohl, Washburn, Bernhardt, Chipman and Francoeur2010) studied arthropods at John F. Kennedy International Airport and found that the structure and composition of the vegetation community affected the richness and diversity of arthropods.
The ground cover at Tianjin Binhai International Airport and the complex surrounding habitats (many farms, ponds, bushes, etc.) provide a considerable breeding and resting habitat for insects and attract a large number of birds to forage. Therefore, from the perspective of the avian food chain, removing the food source of the birds requires controlling the diversity and abundance of insects. Plant species richness and plant composition have been reported to influence insect abundances and diversity (Haddad et al., Reference Haddad, Tilman, Haarstad, Ritchie and Knops2001). The insect communities at airports can be regulated without pesticide use by management of the vegetative cover, ensuring low environmental impact. In the present study, turf vegetation (tall fescue and ryegrass), which was not present in the original habitat at the Tianjin Airport, was established and two control measures, i.e., single-species turf establishment and mowing, were adopted to reduce the species diversity, vegetation height and biomass of ground cover around the airport. The purpose of this study is to explore the effect of vegetation management on insect abundance and diversity and to provide a scientific basis for the ecological control of insects at airports.
Materials and methods
Study site
The study area was the flight zone with ground cover near the southwest runway of Tianjin Binhai International Airport (117°20′48″ E, 39°07′28″ N, altitude 3 m). The area has a warm temperate semihumid continental monsoon climate with a mean annual temperature of 11.8°C, an average annual rainfall of 598 mm and 188 frost-free days. The vegetation is a wild native herb community, including Lagopsis supina, Hemistepta lyrata, Heteropappus altaicus, and Chenopodium glaucum. The area has many species of insects, and the abundance of insects varies significantly with the seasons. Insects are highly active in summer, whereas only a few arthropods such as spiders remain active in winter. The birds in this habitat mainly include Passer montanus, Pica pica, and Hirundo rustica. The bird community around the airport shows obvious seasonal changes – the species richness, total abundance and diversity index are highest in autumn and lowest in spring.
Experimental design
Ryegrass and tall fescue were selected as the experimental plants for single-species turf establishment. Four areas with a ground cover were randomly selected around the airport, each of which was 15 m × 20 m with a spacing of 2 m. A total of four treatments were established as follows: (1) the control area was ploughed in August 2015, no grass seed was sown, and the vegetation grew naturally without mowing; (2) the mowed area was rolled twice a year, and the vegetation was mowed once every 2 weeks; (3) the tall fescue area was ploughed with 50 trenches at a spacing of 0.3 m at the same time as the control area and then sown with 10 kg of tall fescue seeds; (4) the ryegrass area was ploughed and sown with ryegrass seeds in the same manner as the tall fescue area. During the experimental period, the four treatment areas were managed using routine measures without the application of any chemicals. In the tall fescue area and the ryegrass area, the ears of the tall fescue and ryegrass were removed 3 times, in April, May, and June of 2016.
Insect sampling
Insects were sampled twice a month in spring (March–May), summer (June–August), and autumn (September–November) of 2016. Three sample plots (1 m × 1 m each) were randomly chosen in each treatment area. The insects were sampled using a standard sweep net (Evans et al., Reference Evans, Rogers and Opermann1983; Zhu et al., Reference Zhu, Wang, Wang, Bai, Fang and Liu2012). When using the net to capture the insects, the same person swept the net 6 times within each plot with the same strength and amplitude. The collected insects were placed in bottles containing 75% alcohol, and some large lepidopteran insects were placed in triangular bags and brought back to the laboratory for species identification and weighing. The sampled insects were identified to the species level. The collected insects were then placed in alcohol to remove the soil residue, patted dry with filter paper and weighed.
Data analysis
The insect community indices were calculated using the following formulae: Shannon–Wiener diversity, H′ = −Σpi㏑pi; Margalef richness, D = (S−1)/ln N; Berger-Parker dominance, C = Nmax /N; Pielou evenness, J = H′/lnS, where pi is the proportion of the ith genus, N is the total number of individuals in a community, S is the total number of genera, and Nmax is the number of dominant species (Han et al., Reference Han, Ma, Cao, Zhang and Wang2013; Hauptfleisch and Dalton, Reference Hauptfleisch and Dalton2015).
The data are presented as the mean ± standard deviation and were analyzed using SPSS 17.0 statistical software. A one-way analysis of variance followed by Duncan's multiple range test was used to compare the differences among treatments at a significance level of P < 0.05.
Results
Insect community composition and biomass
A total of 1886 insects representing 29 species, 23 families and 8 orders were collected in the four experimental areas (tables 1 and 2). The insect community was dominated by Lepidoptera, Coleoptera, Diptera, and Orthoptera. The main dominant species included Acrida cinerea and Locusta migratoria manilensis (Orthoptera), Propsilocerus akamusi (Diptera), Cicadella viridis and Schizaphis graminum (Hemiptera), and Coccinella septempunctata and Opatrum subaratum (Coleoptera). The coleopteran families (5) and species (7) accounted for the majority (21.7 and 24.1%, respectively) of the total number of families and species. Orthoptera had the highest abundance (573) among the captured insects, accounting for 30.4% of the total; of these, A. cinerea insects were in large numbers, which accounted for 15.2%, followed by L. migratoria manilensis, Teleogryllus emma, Oedaleus infernalis, and Calliptamus abbreviatus. Neuroptera had the lowest species richness and abundance, accounting for 3.4 and 3.6% of the total, respectively; only 68 Chrysoperla sinica were captured. A comparison of the four experimental areas showed that the species richness of insects captured in the control area was 30, which was highest among all the areas, and the insect species in the mowed area, the tall fescue area and the ryegrass area were 5, 6, and 8, respectively.
Insects captured in the sample areas at Tianjin Binhai International Airport
The insect community composition in the sample areas at Tianjin Binhai International Airport
Vegetation management regimes significantly influenced insect populations (table 3). The total numbers of insects captured in the mowed area and the turf area were significantly less than that in the control area, particularly for the ryegrass area, which had 57 individuals per m2, which was 48 individuals per m2 fewer than in the control area. The dominant species in all areas belonged to Orthoptera, and most of which were A. cinerea and L. migratoria manilensis. The number of orthopteran insects in the turf areas was significantly less than that in the control area, with the population in the ryegrass area decreased by 46.5% compared with the control area. In contrast, no significant effect of mowing on the numbers of orthopteran insects was observed. The smallest numbers of insects captured in all areas were neuropteran, and the numbers captured were not significantly different among the different areas.
Abundance of insects in different areas at Tianjin Binhai International Airport
Different lowercase letters indicate significant differences in different areas (P < 0.05).
Significant differences in insect biomass were observed between the turf area and the control area, but there was no significant difference between the mowed area and the control area (table 4). Compared with the control area, the insect biomasses of the tall fescue and ryegrass areas were decreased by 38.5 and 48.5% (P < 0.05), respectively. The taxa with the largest biomasses belonged to Orthoptera, Hymenoptera, and Odonata, particularly A. cinerea and L. migratoria manilensis (Acrididae), Apis cerana (Apidae), and Pantala flavescens (Libellulidae). The biomasses of these three orders in the ryegrass area were significantly lower than those in the control area by 39.8, 65.8 and 91.9%, respectively.
Insect biomass in different areas at Tianjin Binhai International Airport
Different lowercase letters indicate significant differences in different areas (P < 0.05).
The abundance and biomass of insects in different seasons
The abundance and biomass of insects in different areas showed differential seasonal dynamics (fig. 1). The abundance and biomass of insects were significantly higher in summer compared with those in the other two seasons and accounted for 66.2% of the total insect abundance and 77.3% of the total insect biomass. Insect abundance was lowest in autumn. The numbers of O. subaratum, Harpalus sinicus, P. akamusi, and S. graminum were high in spring, but their biomasses were very small. In the fall, with the decrease in temperature, the abundance and species richness of insects were greatly reduced; in particular, Popillia indgigonacea (Coleoptera), Apis cerana (Hymenoptera), and C. sinica (Neuroptera) were sharply reduced in abundance or were absent. Only a small number of orthopteran insects of large body size and biomass remained.
Abundance and biomass of insects in different seasons. The data are reported as the means ± SE. Different lowercase letters indicate significant differences between different treatments within each season (P < 0.05). Different uppercase letters indicate significant differences between seasons within each treatment (P < 0.05).
In spring, the abundance and biomass of the insects in the turf areas were significantly lower than those in the control area, whereas the differences between the mowed area and the control area were not significant. In summer, mowing and turf establishment significantly decreased insect numbers; in particular, the ryegrass area had 38 individuals per m2, which was 32 individuals per m2 fewer than that of the control area. Moreover, the insect biomasses of the tall fescue and ryegrass areas decreased by 38.0 and 48.2% (P < 0.05), respectively, compared with the control area. In autumn, the abundance of insects in the ryegrass area was significantly lower than that in the control area. However, no significant differences were found between the other two treated areas and the control area, and insect biomass was not influenced by mowing and turf establishment in autumn.
The insect community indices
The richness (D) and diversity (H’) indices fluctuated across all seasons in the different areas (table 5). Except for the mowed area, a higher richness was observed in summer than in the other two seasons (P < 0.05). In spring, the richness index of the turf area was significantly lower than that of the control area, whereas no significant differences were found between the mowed area and the control area. In summer, significant decreases in richness index were observed between the three managed areas and the control area. In autumn, there were no distinct differences in the richness index among the four areas.
Community indices of insects in different seasons and areas at Tianjin Binhai International Airport
Different lowercase letters indicate significant differences between different treatments within each season (P < 0.05). Different uppercase letters indicate significant differences between seasons within each treatment (P < 0.05).
In all areas, the diversity index was highest in summer, followed by spring and autumn. In spring, the turf areas had a lower diversity index than the control and the mowed areas, but the difference between the mowed area and the control area was not significant. In summer, mowing and turf establishment significantly decreased diversity compared with the control area. In autumn, no significant differences in diversity index were observed among the four areas.
Discussion
The insect community in the experimental area of Tianjin Binhai International Airport was mainly composed of members of Orthoptera, Lepidoptera, Diptera, and Coleoptera. Orthoptera and Coleoptera were dominant in abundance, whereas Orthoptera and Hymenoptera were dominant in biomass. The abundance and biomass of insects changed with the seasons, and both were significantly higher in summer, mainly due to the higher temperature and adequate rain in summer, which are conducive to insect reproduction and growth (Zhu et al., Reference Zhu, Wang, Wang, Fang, Sun and Ren2014), particularly the massive reproduction and rapid increase in biomass of A. cinerea, L. migratoria manilensis, O. infernalis, and C. abbreviates (Orthoptera). The composition and dominant species of the insect communities was similar in the different areas. The dominant species in the turf areas were A. cinerea, P. akamusi, S. graminum, and C. viridis, and the dominant species in the mowed area and the control area were A. cinerea, P. akamusi, P. indgigonacea, and C. septempunctata. This difference may be related to the small area compared with the large range of insect activities. Spatial scale is an important feature of landscape patterns. Large-scale changes in landscape patterns around the airport can directly affect the distribution and spread of insects and can even hinder the migration of insects (Ge et al., Reference Ge, Ouyang and Men2017).
Compared with the control area, the abundances of insects in the three treated areas were significantly decreased, and species richness was also decreased. These data indicate that ground cover management was conducive to a reduction in species richness and abundance of insects in the airport ecosystem, particularly Pieris rapae, P. flavescens, Ambrostoma quadriimpressum, and Popilia indgigonacea; the abundances of these species were significantly reduced. Within the airport ecosystem, vegetation, insects, birds and their surroundings interact and restrict each other and form an ordered entity through material circulation and energy flow. Starting from this perspective, two measures – mowing and single-species turf establishment – were adopted to adjust and control the vegetation-insect-bird food chain within the ecosystem, resulting in major changes in the habitat. Some insects have poor adaptability, which can lead to a decline in their population density with habitat change. Changes in insect populations may reduce the number and species of birds and thus potentially prevent the occurrence of birdstrikes.
Insects are susceptible to disturbance and vegetation conditions. The plant community is an important driving force affecting the abundance and diversity of the insect community (Kruess and Tscharntke, Reference Kruess and Tscharntke2002; Zhao et al., Reference Zhao, Reddy, Wei, Zhu, Zhang, Yu, Wang, Jiang and Zhang2018). In this study, the diversity of the vegetation community had a significant effect on the abundance and diversity of insects and confirmed that the greater the species richness of the vegetation, the more complex the insect community and the higher its diversity. The turf areas created a uniform vegetation community with lower vegetation coverage and diversity than the control area, and the abundance, biomass, and diversity of insects were also reduced, indicating that turf establishment had a strong inhibitory effect on insects, particularly on certain pollinating insects such as Pieridae (Lepidoptera) and Apidae (Hymenoptera). These observations are consistent with the results reported by Bronstein et al. (Reference Bronstein, Alarcon and Geber2006), who found that the species richness and abundance of insects decreased with a decrease in plant diversity. Jonas et al. (Reference Jonas, Whiles and Charlton2002) and Haddad et al. (Reference Haddad, Tilman, Haarstad, Ritchie and Knops2001) studied the relationship between insects and plant diversity and found that the species richness of herbivorous insects was correlated with plant species richness and they believed that plant species richness determined insect species richness. Wenninger and Inouye (Reference Wenninger and Inouye2008) also found that insect diversity and abundance were positively correlated with plant diversity. Mowing is a rapid and effective way to reduce plant height and biomass. As the frequency of mowing increases, competition with some tall plant species (such as Eleusine indica, E. crus-galli, and Imperata cylindrica) decreases, and the richness of the vegetation community decreases, resulting in an insufficient nutritional supply for insects, reduced space for insect feeding and habitation, and a decreased richness in the insect community. The present study showed that the abundance of insects in the mowed area was significantly lower than that in the control area, which was consistent with the results reported by Liu and Zhou (Reference Liu and Zhou2004). Noordijk et al. (Reference Noordijk, Schaffers, Heijerman, Boer, Gleichman and Sýkora2010) showed that proper mowing reduced the diversity and richness of arthropods. Brigitte et al. (Reference Brigitte, Lorenzo, Gheinrich and Bruno2009) also confirmed that mowing reduced the abundance of grasshoppers.
Studies have shown that alien plants are less susceptible to pest damage than native plants, are less attractive to insects, and can suppress insect abundance (Lau and Strauss, Reference Lau and Strauss2005; Kirichenko and Kenis, Reference Kirichenko and Kenis2016). Around airports, the establishment of ryegrass, with its developed fibrous roots and strong tillering ability, and tall fescue, with its high cold resistance, adaptability, and disease resistance can inhibit the growth of native plants and reduce the diversity of ground cover vegetation when combined with management measures. Moreover, the establishment of non-native turf species can indirectly affect the local food network (Heard and Sax, Reference Heard and Sax2013; Avanesyan and Culley, Reference Avanesyan and Culley2015). Alien turf vegetation changes the structure of trophic groups, which may reduce the attractiveness to birds that feed on grass leaves and seeds (such as Anser fabalis serirostris, Anas poecilorhyncha, and P. montanus). In addition, despite a small number of weeds (such as H. altaicus, Conyza canadensis, and L. supina) that have weak growth and are low in height and density, turf establishment makes the vegetation community less complex, which has a controlling effect on some dominant insect species with large biomasses and thereby reduces the attraction of carnivorous and omnivorous birds (such as Lanius schach, Cuculus canorus, and Hirundinidae). Therefore, single-species turf establishment can effectively control the vegetation and insect trophic levels in the vegetation-insect-bird food chain by affecting the normal feeding of some insects and their insect predators; in turn, the abundance and species richness of insects is reduced, thus eliminating food sources for some birds, which is conducive to reducing the appearance of birds around airports.
In summary, ground cover management at Tianjin Binhai International Airport, including mowing and single-species turf establishment, reduced the abundance, species richness, biomass, and diversity of insects and the effects were strongest in the areas where ryegrass was established. Therefore, it is recommended to plant single-species turf vegetation on a large scale around airports and to adopt appropriate management measures such as mowing or rolling to decrease the abundance and diversity of insects, thus reducing bird populations at airports.
Acknowledgements
The authors sincerely thank Tianjin Binhai International Airport for financial support and for providing the experimental site. They also thank American Journal Expert (AJE) for its linguistic assistance during the preparation of this manuscript.
Conflict of interest
The authors declare that they have no conflict of interest.
Ethical standards
This article does not contain any studies with human participants or animals performed by any of the authors.
