Research Article |
Corresponding author: Ekaterina Kozuharova ( ina_kozuharova@yahoo.co.uk ) Academic editor: Vlada Peneva
© 2022 Ekaterina Kozuharova, Vasil Simeonov.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kozuharova E, Simeonov V (2022) Monitoring bumblebee pollinator visits to the medicinal plant Gentiana asclepiadea L. (Gentianacese) – a comparison between the periods 1990–1994 and 2017–2020. In: Chankova S, Peneva V, Metcheva R, Beltcheva M, Vassilev K, Radeva G, Danova K (Eds) Current trends of ecology. BioRisk 17: 317-327. https://doi.org/10.3897/biorisk.17.76577
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Ever increasing data continue to indicate the decline of bumblebee populations. The key factors causing declines in their abundance and diversity are: 1) habitat destruction, 2) loss of floral resources, 3) emerging diseases, 4) increased use of pesticides (particularly neonicotinoids).
The aim of this study is to monitor bumblebee visits to Gentiana asclepiadea L, recording pollinator species, and taking measurements of seed set. This plant species is chosen for two reasons: 1) similar data is available from our previous research in the 1990’s and 2) this montane plant species is supposed to be less exposed to hazards from pesticides and habitat destruction. Three study sites were chosen in Mt. Vitosha (SW Bulgaria) where natural populations of G. asclepiadea occur in 1990. The observations of bumblebee activity in the flowers of G. asclepiadea were conducted during the flowering seasons (August and September) of 2017 – 2020 at the same study sites and compared to the data obtained in the previous period (1990–1994). The free pollination fruit set was tested by monitoring of 100 G. asclepiadea flowers each year for development of fruit capsules. The seed set was tested by counting the matured seeds and non-fertilised ovules of 10 fruit capsules each year. A slight decline in bumblebee activity was recorded in 2017 – 2020 in comparison to 1990–1994. This is reflected in the fruit set and the seed set. Our data demonstrates that even in a mountain habitat, where there are fewer direct hazards to bumblebees, that pollination effectiveness has been suppressed over time. This corresponds to a research study which provides evidence that insect biomass fell by 76% in German nature reserves between 1989 and 2016.
Bombus, bumblebees decline, monitoring, pollinators
Pollinators are a crucial element of biodiversity, since the majority of plant species depend on them for reproduction by seed. However, ever increasing data indicate that pollinating insects, and in particular bumblebees, are in decline. The key factors causing declines in their abundance and diversity are: 1) habitat destruction; 2) loss of floral resources; 3) emerging diseases; 4) increased use of pesticides (particularly neonicotinoids) (
For the conservation of wild pollinators, long-term monitoring is necessary (
There is no long-term quantitative data about bumblebees in Bulgaria. An efficient approach is by monitoring pollinator visits to one or more plant species, ideally recording pollinator species and also taking seed set measurements (Goulson, personal communication). A good candidate is Gentiana asclepiadea L. for two reasons: 1) such data is available from our previous research in the 90’s of the last century; 2) this montane plant species is supposed to be less exposed to the hazards such as pesticides and habitat destruction.
Gentiana asclepiadea is a perennial plant. The rhizome is more or less thick and branched. There are sterile and usually several fertile stems, which are straight, nonbranched and 35-50 (80) cm tall. There are 1-3-5-merous flowers sitting in nodes, at the base of the leaves. They are of the funnel type. Their size varies between (35) 40-50 mm and the corolla lobes are 3-4 times shorter than the corolla tube (
The aim of this case study is to monitor bumblebee visits to G. asclepiadea, recording pollinator species, and also taking seed set measurements.
Three study sites were chosen (
Study sites in Vitosha Mts., SW Bulgaria as follows: site 1 – 42°36'13.2"N, 23°15'04.0"E, site 2 – 42°36'20.5"N, 23°17'39.4"E, site 3 – 42°34'05.1"N, 23°17'52.6"E Study sites 1 and 2 were in open woodlands in the coniferous forest belt. Study site 3 was in the subalpine meadows just above the coniferous forest belt.
The field investigations were conducted during the flowering seasons (August and September) of 1990–1994 (
The field observations were conducted over 66 hours during 48 days in different meteorological conditions. The visiting bumblebees were identified in the field. Their visitation rate and behaviour in the flowers were recorded. Since the focus of this study was mainly on visitation rate, we refrained from further collection of specimens as this would affect the results. Although Bombus wurflenii (Radoszkowski, 1860) and B. lapidarius (L., 1758) belong to different subgenera (Alpigenobombus and Melanobombus) and ecologically, they are different (B. lapidarius is distributed everywhere, while B. wurflenii is a montane species) it is hard to distinguish with certainty between these two species in the field as their colours are the same. Also, it is hard to distinguish B. hortorum (L., 1758) from B. subterraneus ssp. latreillellus (Kirby), and B. lucorum (L., 1758) from B. terrestris (L., 1758) in the field. Therefore, we preferred the approximate approach rather than irrelevant “precision” and in the result and discussion parts they appear as undistinguished pairs B. wurflenii and/or B. lapidarius, B. hortorum and/or B. subterraneus, B. lucorum and/or B. terrestris. A pollinator activity index was calculated as the quotient of the number of pollinators recorded and the minutes of observation multiplied by 60 minutes. The most numerous plants flowering simultaneously in the neighbourhood and their bumblebee visitors were recorded.
A Linear regression analysis of the total activity of bumblebees at each study site against the time/years of observation was applied to test the trend in the bumblebees’ activity. The sequence of years of observations has a serious interruption (from 1994 to 2017) and thus the model does not allow prediction. It is just informative, rather qualitative than quantitative. Therefore, we refrained from Linear regression analysis of each bumblebee species’ activity during the period of observations as well as the fruit and seed set.
The free pollination fruit set was tested by monitoring 100 flowers of G. asclepiadea each year for development of fruit capsules. The seed set was tested by counting the matured seeds and non-fertilised ovules of 10 fruit capsules. The damage inflicted by insect predators on the maturing seeds was not calculated for this research (see
Since the flowering period of the observed foraging plant is late summer and early autumn, we were observing the latter part of bumblebee colony activity. The species composition of the bumblebees visiting the flowers of G. asclepiadea remains basically the same over time. It is as follows: Bombus pascuorum (Scopoli, 1763), B. wurflenii /B. lapidarius, B. pratorum (L., 1758), B. hortorum /B. subterraneus ssp. latrellellus, B. terrestris and B. lucorum. The bumblebee activity varied over the years as well as within the study sites (Figs
Even though the linear regression model is just informative and not suitable for prediction, decreasing trends are observed at all three study sites (Figs
Peculiarities which cannot be detailed in the charts are worth noting. In the first days of September 1991 high activity of B. hortorum/B. subterraneus males was recorded in the flowers of G. asclepiadea, at site 1, where they were feeding on nectar (
The free pollination fruit set tested by counting fertilised fruits versus flowers that failed to set fruit, as well as the seed set tested by counting the matured seeds and non-fertilised ovules, are presented on Fig.
A Bombus hortorum/subterraneus collecting nectar in 1991 at site 1 B B. wurflenii/lapidarius worker robbing nectar of Gentiana asclepiadea in 2017 at site 2 C B. wurflenii/lapidarius worker taking nectar from a male stage flower in 2017 at site 2 D B. wurflenii/lapidarius and pollinating Epilobium angustifolium at site 3.
A fluctuation in bumblebees’ activity within the years and the study sites was observed. Such fluctuation in bumblebees’ activity seems to be a normal process depending on several factors including colony initiation, pathogens, parasitoids, predators, food resources and landscape etc. (
The observed fluctuations in pollinator activity are related to the study sites where observations were performed. It is quite interesting that, in general, fewer bumblebees were recorded at study site 3 – subalpine meadows. At this site Epilobium angustifolium L. and Solidago virgaurea L. had large populations and these possibly over-competed for bumblebee pollinators. Bumblebees are known to favour S. virgaurea (Teräs, 1976). And E. angustifolium was observed to attract a lot B. wurflenii/B. lapidarius and B. pratorum (Fig.
The high activity of B. hortorum/ B. subterraneus ssp. latreillellus males feeding on nectar in the flowers of G. asclepiadea during the first days of September can be explained by their phenology (
The slight decline of bumblebees’ activity recorded in 2017–2020 in comparison to 1990–1994 reflected on the fruit set and the seed set. Our data demonstrate that even in a mountain habitat with fewer direct hazards for bumblebees a negative effect on pollinator activity over time is still detectable. Our results correspond to a research study which provides evidence that insect biomass fell by 76% on German nature reserves between 1989 and 2016 (
We are grateful to Prof. A.J. Richards for the English language editing and the useful comments. Special thank you to Dr. Andrej Gogala and Biljana Stoykova for the useful comments about bumblebee identification.