A new species-specific approach to detect a saproxylic hoverfly pollinator, with implication in forest ecosystems conservation

doi:10.21203/rs.3.rs-1712529/v1

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A new species-specific approach to detect a saproxylic hoverfly pollinator, with implication in forest ecosystems conservation

https://doi.org/10.21203/rs.3.rs-1712529/v1

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Hoverflies play a key role in pollinating and other forest ecosystem services. They can be used as bioindicators of many different habitats. The presence of species with high environmental requirements, especially in forest ecosystems, can be a fundamental tool for developing the right management plan for biodiversity conservation also in an ecological connectivity perspective. Mallota fuciformis Fabricius, 1794 is an elusive saproxylic species listed as threatened in many European countries and internationally recognised as a species of conservation interest. In this paper, we provide for the first time a targeted, fast and effective standardised field protocol for the detection of Mallota fuciformis in oak-hornbeam stands and alluvial forests with oaks along lowland streams. Given the short period of flight of the species, 88 sites were considered enough to testify this standardised methodology. The study was carried out in the Piedmont region (Northwestern Italy) between 2019 and 2022. Overall, 48 sites have proved to be positive for the presence of the species. The average detection time was very short in positive sites, suggesting the effectiveness of this approach in fast surveys. The proposed protocol can be extended to other geographical areas. The possibility to apply the proposed methodology for extensive ecological connectivity studies is discussed.

Implications for insect conservation

To monitor long-term trends of elusive pollinators, ad hoc protocols need to be developed. In this perspective, our work proposes a new monitoring method tested on a target species but applicable to different species of interest. In addition, this method could be further implemented for the assessment of forest network connectivity.

Mallota fuciformis

binocular

ecological connectivity

Piedmont

field protocol

Hoverflies play a key role in pollinating (Doyle et al. 2020; Rader et al. 2020; Chisausky et al. 2020) and other forest ecosystem services (Ricarte et al. 2009; Dunn et al. 2020). They are internationally recognised as excellent bioindicators (Burgio and Sommaggio 2007; Cadotte et al. 2011, Montoya et al. 2021) of functional biodiversity of many different habitats. The presence of species with high environmental requirements, especially in forest ecosystems, can be a fundamental tool for developing the right management plan for biodiversity conservation also in an ecological connectivity perspective. Mallota fuciformis is a saproxylic hoverfly found in deciduous forests with over-mature trees. The elective habitats of the species are represented by Fagus/Quercus forests, Quercus/Carpinus/Ulmus forests with rivers and streams and thermophilous Quercus forest with Populus/Salix along rivers or in wet areas (Speight 2020). The developmental stages are not described, but they probably develop in basal rot-holes containing wet humus (Speight 2020) or in rain-fed temporary water bodies of overmature/senescent trees. The larvae are presumably similar to other congeneric species having a rat-tail shape as they live in trunks filled with water (Krivosheina 2002). It is precisely because of its particular larval needs that Speight (1989) lists M. fuciformis among those species useful in identifying forests of international importance for nature conservation in Europe. M. fuciformis is widespread in Europe although observations are scarce, while outside of Europe it is present only in Iran (Babaei et al. 2019). The scarcity of reports is mainly due to the fact that this elusive species flies in early spring, for a short period of 2-3 weeks which in the Piedmont region matches the second half of March. This is a time of the year frequently overlooked by samplings, which often start around April. Moreover, the species tends to fly high in the canopy making it difficult to be observed in the field. Lastly, in Northwestern Italy, the adults of the species have been observed to be very selective visiting only Prunus flowers. Due to the scarcity of sightings, this hoverfly species is considered threatened in several national red lists: it is regarded as Vulnerable in Germany (Ssymank et al. 2011) and Czech Republic (Mazànek and Bartàk 2005), Endangered in Poland (Zoralski and Kowalczyk 2017). Recently, it was reported for the first time in Slovenia, Serbia and Switzerland (De Groot and Janevic 2020; Nedeljkovic et al. 2009, Pennard pers. comment), while for other countries most records date back to more than 100 years ago (France - Speight et al. 2018; Italy - Birtele pers. comment). Nevertheless, the recent IUCN assessment states Mallota fuciformis in the Least Concern category (Pennard et al. 2021). This is partly due to the recent increase of interest in hoverflies, which has led to more samplings and consequently more observations. Mallota genus is considered one of the most efficient taxa of pollinators in natural ecosystems (Chisausky et al. 2020) thanks to their bumblebee-like morphology presenting dense and long hairs. For all these reasons, Mallota fuciformis is among those rare and threatened species for which the proposed EU pollinator monitoring scheme advocates the development of specific methods to complement the minimum viable scheme (Potts et al. 2021).

In Italy, the knowledge on the distribution of the species prior to this study was very scarce, with less than 10 known sites. Within the Piedmont region the only information we have comes from some specimens collected during the 19th century (Sommaggio 2007) and few recent findings (Maritano 2020; 2021). In this framework, the main goals of this paper are:

(1) To provide a species-specific monitoring protocol.

(2) To increase the knowledge on the distribution of Mallota fuciformis in the Piedmont region.

(3) To propose this species as a bioindicator of the ecological connectivity of forest networks.

Survey area

The study area is the Piedmont region (Northwestern Italy). This region has very few data available on M. fuciformis and, in contrast, it shows a large portion of territory with habitats suitable for the species. The main habitats investigated are oak-hornbeam stands and alluvial forest with oaks along lowland streams up to 670 m a.s.l. The investigated woods have been chosen from the Forest Chart (I.P.L.A. 2008) by selecting oak type vegetation and starting from the widest and most uniform areas up to the smaller ones. In areas where there were many separated small forests, a single point was chosen to represent the entire metapopulation. In these cases, it was preferred to investigate the more isolated sites than those possibly connected with other forests already investigated. Some additional sites have been chosen along stretches of rivers with presence or absence of oaks in order to test the monitoring method.

Species Identification

Mallota fuciformis is well distinguished from other hoverflies by macroscopic features that are easily observable even with the naked eye (e.g. body-hair colour, general morphology). It may be confused with some bumblebee-like species of the genera Volucella, Criorhina, Eriozona or Sericomyia, but fortunately only a few of these fly in March, so misidentifications are very improbable. The species most likely to confuse an inexperienced eye is Criorhina ranunculi. In fact, C. ranunculi can show different morphotypes, one of them with reddish hair at the end of the abdomend, somewhat similar to those of Mallota fuciformis. For this reason, in case of doubt, it is recommended to observe the facial profile, which in C. ranunculi is very protruding and has whitish stripes. Furthermore, in contrast to the target species, in C. ranunculi the hind femurs of males are thickened and the wings often overlap when it is sitting on a flower. Mallota fuciformis is therefore an easily recognisable species in the field even without capture.

Data Collection For Protocol Development

There are many different sampling techniques proposed by literature that can be used to detect insects in natural ecosystems (Vrdoljak and Samways 2012; Löcken et al. 2020; Karlsson et al. 2020). Malaise trap, pan traps and entomological net transects are commonly used for sampling hoverflies (Campbell and Hanula 2007; Burgio et al. 2015; Maritano 2021; Sommaggio et al. 2022), but for species-specific searches, the development of ad hoc protocols that maximise the expected results is advisable. In this way, it is possible to save time and money while simultaneously reducing the amount of unnecessary material collected.

In order to develop a standardised method for the detection of Mallota fuciformis in forest ecosystems, we proceeded as follows. We carried out 120-minute observation points in front of flowering Prunus plants. Observations were carried out by sight or with the aid of binoculars in the case of tall trees or for plants that were not easily reachable. The observation points were carried out between 10 a.m. and 5 p.m. on sunny, windless days from the 15th to the 31st of March. Each point was independent and set inside or in the ecotone of the woodland investigated. As soon as the observer clearly saw a specimen of Mallota fuciformis the session ended as the site was considered positive for the presence of the species. Conversely, if no sightings had been made during the two hours, the session ended and the site was considered negative. In cases where a possible specimen of Mallota fuciformis was observed, but without certainty (because it flew very fast, because it was partially hidden from view, etc.), the site was considered doubtful. In addition, during the monitoring session it was possible to record the presence of other interesting saproxylic hoverflies belonging to the genera Brachypalpus, Brachyopa or Criorhina.

Data analysis

The analyses of the collected data, shown in the results section, were carried out using the RStudio software (Version 1.4.1106).

Overall, 88 sites (see Supplementary material) have been inspected by five observers (including the authors), specifically trained to recognize Mallota fuciformis (see Fig. 1). The species was sighted at 48 sites, while another 2 sites were considered doubtful for its presence. The remaining 38 sites were considered negative, as no specimens were sighted. M. fuciformis has been detected in most of lowland oak-hornbeam remnants including sites of limited extension such as parks of historic royal palaces. It is well spread in meso-igrophilic forests with Quercus, Salix and Fraxinus even in pre-mountain areas, while along rivers it is only found in the most intact portions of woodland.

As shown in Fig. 2a, all sightings occurred within 60 minutes, with only five outliers occurring much later. The mean detection time is 25 minutes (see the yellow triangle in the boxplot in Fig. 2a), a very short time interval for a canopy species. The median falls at 11.5 minutes, meaning that half of the sightings occurred within this very short period of time. Applying a Wilcoxon rank sum test, we have not observed any significant difference in the detection time between sites investigated during the morning (10:00 a.m. − 01:30 p.m.) compared to sites investigated in the afternoon (01:30 p.m. − 05:00 p.m. - see boxplots in Fig. 2b)

If many flowering Prunus are present at the site under investigation, there may be a 'dilution effect'. As the species maintains itself at low densities, the presence of many plants where it can feed makes its observation more difficult. In these instances, the detection time may increase considerably, or the species may not be detected at all despite its presence. In fact, in only 2 out of 48 surveys more than one specimen was observed on the same plant. In these cases, the Prunus surveyed was the only one present near the potential breeding site. Observations have shown that Mallota fuciformis stays on the Prunus flowers for a very short time, hardly more than 1–2 minutes, then flies away and eventually returns after 10–15 minutes.

Other saproxylic hoverfly species were observed during the monitoring sessions: Criorhina ranunculi (32 sites), Criorhina floccosa (5 sites), Brachypalpus sp. (15 sites), and Brachyopa sp. (2 sites). Even if in most field observations these species coexisted peacefully, aggressive interspecific interactions were sometimes observed towards Criorhina ranunculi or Bombus sp. specimens in order to defend the trophic resource.

In order to assess the influence of the forest extension on the presence of Mallota fuciformis, we divided the investigated sites into small (< 25 ha), medium (25–100 ha) and large (> 100 ha) ones. As shown in the graph in Fig. 3, the presence of the species is influenced by the size of the forest investigated in a statistically significant way. To compare the frequencies of observation, Pearson’s chi-square test was used. The test applied to large and small sites showed a p-value = 0.004, whereas when applied to large and medium sites it showed a p-value = 0.003. In contrast, the differences in frequency of observation between medium and small sites did not give a significant result.

Proposed Monitoring Protocol

In accordance with the results obtained, the following monitoring protocol is proposed.

The sampling site must be chosen taking into account M. fuciformis’s habitat preferences, as well as the fact that it can be found even in small wooded areas (< 25 ha). The presence of flowering Prunus is a necessary element without which surveys cannot be carried out. For the Piedmont region, the protocol’s application period is strictly confined to the second half of March, but it may vary slightly depending on the climatic characteristics of the territories under study. The only exception for the Piedmont region is the Susa Valley with its xeric microclimate where Prunus plants bloom sooner and the target species flies in early March. The selection of Prunus must be made carefully because it can affect the results. It must be as close as possible to the forest under investigation and as far away as possible from other blooming Prunus in order to avoid the ‘dilution effect’.

The optimal Prunus species for the monitoring is Prunus cerasifera, but if it is not present in the area of interest then Prunus spinosa may be chosen. Prunus avium should be avoided if taller than 4 metres.

Since Mallota fuciformis flies during the warm hours of the day, monitoring should only be started when the air temperature has reached at least 13°C and in any case never before 10:00 a.m. Furthermore, monitoring can only be carried out if at least part of the Prunus is directly illuminated by sunlight. In case of passing clouds, the time count can be stopped and resumed as soon as the sun returns. The presence of other flying Diptera may give an indication of whether the correct conditions for the application of the monitoring protocol are met. For the same reasons related to temperature and light, observations cannot be extended beyond 5 p.m. If the monitoring protocol is applied in different parts of Europe, the aforementioned timetables may vary accordingly.

We propose an observation time of 60 minutes. Observations should be carried out by direct sight and with the aid of binoculars in order to assure a fast field identification.

Update of the distribution map of Mallota fuciformis in the Piedmont region

Thanks to the surveys carried out to test the monitoring protocol, the knowledge on the distribution of Mallota fuciformis in the Piedmont region has been greatly increased. As can be seen from Fig. 4 (left), prior to this study, the species was only known to occur at 4 sites: Stupinigi and Turin (thanks to Bellardi's collection dating back to the second half of the 19th century - Sommaggio 2007), ‘Bosco del Merlino’ Nature Reserve (Caramagna Piemonte, CN - Maritano 2020) and ‘Bosco delle Sorti della Partecipanza’ (Trino, VC - Maritano 2021). In contrast, 50 sites have now been confirmed for the presence of M. fuciformis in Piedmont (Fig. 4, right). Of these 50 sites, 2 were added thanks to observations uploaded to the citizen science platform iNaturalist. The attached photos allowed the correct identification of the species and therefore the 2 observations were validated by the authors of this article.

To give an idea of the increase in knowledge about the distribution of the species in the region, the Extent of Occurrence (EOO) was calculated. Prior to this study, the EOO was 715 km², while it now amounts to 13.481 km².

The monitoring protocol proposed here is a specific approach developed in a framework derived from the proposal for an EU Pollinator monitoring scheme (Potts et al. 2021) which advises species-specific protocol for rare and threatened species. The strengths of this protocol are:
- it can easily be applied by non-expert operators following a very short training session;
- it does not involve the killing of any specimens to collect data;
- it is very efficient, as it allows the target species to be observed in a short period of time.
A critical point in this protocol is certainly the choice of Prunus tree on which to carry out the observation. In fact, the Prunus tree must be chosen wisely and carefully because some of its characteristics (e.g. exposure to sunlight, status of inflorescence, position relative to the forest, position relative to other Prunus trees) can influence the monitoring results. The field application of this method has confirmed its high effectiveness. Thanks to its use, the knowledge on the distribution of Mallota fuciformis in the Piedmont region has increased considerably. The proposed monitoring protocol can be extended to different geographical areas by making the necessary adjustments (e.g. time of year, monitoring times, plants on which observations can be made). In addition, it could be used as an example for the development of similar protocols, but targeted at other saproxylic species of interest e.g. Criorhina floccosa. Finally, this protocol can be used in long-term pollinator monitoring.

A further use of this methodology could concern the assessment of the ecological connectivity of lowland forest networks. Since, in recent centuries, the lowland forests of Piedmont have been affected by a dramatic decrease (Camerano et al. 2009) mainly due to land use changes (urbanisation, agriculture and invasive species), the development of ecological networks capable of ensuring connectivity to the residual remnants has become of primary importance for land management. To achieve this goal, it is necessary to enhance or preserve forest ecosystems along streams edges. In this framework, the presence of M. fuciformis in well-defined forest portions along river stretches can be used as a bioindicator of the presence of adequate functional forest continuity.

Conflict of interest
The authors have no competing interests to declare that are relevant to the content of this article.

Authors contribution
Conceptualization, UM; methodology, UM, LB; formal analysis, LB; investigation, UM, LB; writing-original draft preparation, UM, LB; writing-review and editing, UM, LB. All authors have read and agreed to the published version of the manuscript.

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

Acknowledgement
We sincerely want to thank Guido Doglione, Michela Ermellino and Luca Liprandi for their invaluable involvement in field activities.

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No competing interests reported.

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A new species-specific approach to detect a saproxylic hoverfly pollinator, with implication in forest ecosystems conservation

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Abstract

Figures

Introduction

Materials And Methods

Survey area

Species Identification

Data Collection For Protocol Development

Data analysis

Results

Proposed Monitoring Protocol

Discussion

Statements And Declarations

References

Additional Declarations

Supplementary Files

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