PAOLO BIELLA

University of Milano Bicocca, Biotechnology and Biosciences, Research Fellow

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Papers by PAOLO BIELLA

City climate and landscape structure shape pollinators, nectar and transported pollen along a gradient of urbanization

Journal of Applied Ecology, 2022

This is an open access article under the terms of the Creative Commons Attribution License, which... more

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Investigating pollination strategies in disturbed habitats: the case of the narrow-endemic toadflax Linaria tonzigii (Plantaginaceae) on mountain screes

Plant Ecology, 2021

Plant mating systems may reflect an adaptation to a habitat type, with self-pollination being pot... more Plant mating systems may reflect an adaptation to a habitat type, with self-pollination being potentially common in unstable and disturbed conditions. We investigated the reproductive ecology of an Alpine, narrow-range toadflax, Linaria tonzigii Lona (Plantaginaceae), occurring in steep and dynamic mountain screes. We explored self-compatibility and spontaneous autogamy, seed viability, daily nectar production, pollinator behaviour and pollen transfer in wild populations, using hand pollination treatments, quantification of nectar volume, viability Tetrazolium assay, active pollinator sampling and video recordings, and UV-bright dust for pollen substitution. After ex novo sequencing of several genetic regions of L. tonzigii, we performed a multi-marker phylogenetic analysis of 140 Linaria species and tracked the occurrence of the self-compatibility trait. Our results showed that this species is self-compatible, pollinated mostly via spontaneous auto-gamy and pollinator-mediated geitonogamy, and self-pollinated seeds are as viable as cross-pollinated ones. Selfing could be due to pollinator rarity because, despite the studied species providing a high nectar volume, wild bees, moths and small beetles infrequently visited its flowers in the sparsely vegetated Communicated by Marjana Westergren. Supplementary Information The online version contains supplementary material available at https://doi.

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Niche differences may explain the geographic distribution of cytotypes in Erysimum mediohispanicum

Plant biology (Stuttgart, Germany), Jan 25, 2017

Polyploidization has played an important role in plant diversification, and variation in ploidy l... more Polyploidization has played an important role in plant diversification, and variation in ploidy level may be found not only between species of the same genus, but also within a single species. Although establishing the adaptive significance of polyploidy to explain the geographic distribution of cytotypes is challenging, the occurrence of different cytotypes in different ecological niches may suggest an adaptive role of genome duplication. We have studied the adaptive significance of the geographic distribution of cytotypes across the entire distribution range of the endemic Erysimum mediohispanicum (Brassicaceae). For that, we have used climatic variables, population elevation, and soil properties to model ecological niches for the different cytotypes. In addition, we have analysed the effect that ploidy level has on the floral phenotype. We have found a clear geographic pattern in the distribution of cytotypes, with diploid individuals occurring in the southernmost part of the dis...

The cephalic labial gland secretions of two socially parasitic bumblebeesBombus hyperboreus(alpinobombus) andBombus inexspectatus(thoracobombus) question their inquiline strategy

Insect Science, 2016

Socially parasitic Hymenoptera have evolved morphological, chemical, and behavioral adaptations t... more Socially parasitic Hymenoptera have evolved morphological, chemical, and behavioral adaptations to overcome the sophisticated recognition and defense systems of their social host to invade host nests and exploit their worker force. In bumblebees, social parasitism appeared in at least three subgenera independently: in the subgenus Psithyrus consisting entirely of parasitic species, in the subgenus Alpinobombus with Bombus hyperboreus, and in the subgenus Thoracobombus with B. inexspectatus. Cuckoo bumblebee males utilize species-specific cephalic labial gland secretions for mating purposes which have been showed as acting in their inquiline strategy. We performed cephalic labial gland secretions comparative analyses of B. hyperboreus, B. inexspectatus and their hosts. Males of both parasitic species exhibit high species specific levels of cephalic gland secretions, including different main compounds. Our results show no chemical mimicry in the cephalic gland secretions between inquilines and their host and we did not identify the repellent compounds already known in other cuckoo bumblebees. This article is protected by copyright. All rights reserved.

An empirical attack tolerance test alters the structure and species richness of plant-pollinator networks

by PAOLO BIELLA and Jeff Ollerton

Functional Ecology, 2020

1. Ecological network theory hypothesizes that the structuring of species interactions can convey... more 1. Ecological network theory hypothesizes that the structuring of species interactions can convey stability to the system. Investigating how these structures react to species loss is fundamental for understanding network disassembly or their robustness. However, this topic has mainly been studied in-silico so far. 2. Here, in an experimental manipulation, we sequentially removed four generalist plants from real plant-pollinator networks. We explored the effects on, and drivers of, species and interaction disappearance, network structure and interaction rewiring. First, we compared both the local extinctions of species and interactions and the observed network indices with those expected from three co-extinction models. Second, we investigated the trends in network indices and rewiring rate after plant removal and the pollinator tendency at establishing novel links in relation to their proportional visitation to the removed plants. Furthermore, we explored the underlying drivers of network assembly with probability matrices based on ecological traits. 3. Our results indicate that the cumulative local extinctions of species and interactions increased faster with generalist plant loss than what was expected by co-extinction models, which predicted the survival or disappearance of many species incorrectly, and the observed network indices were lowly correlated to those predicted by co-extinction models. Furthermore, the real networks reacted in complex ways to plant removal. First, network nestedness decreased and modularity increased. Second, although species abundance was a main assembly rule, op-portunistic random interactions and structural unpredictability emerged as plants were removed. Both these reactions could indicate network instability and fragil-ity. Other results showed network reorganization, as rewiring rate was high and asymmetries between network levels emerged as plants increased their centrality. Moreover, the generalist pollinators that had frequently visited both the plants targeted of removal and the non-target plants tended to establish novel links more than who either had only visited the removal plants or avoided to do so.

Northwestward range expansion of the bumblebee Bombus haematurus into Central Europe is associated with warmer winters and niche conservatism

by PAOLO BIELLA, Aleksandar Cetkovic, Andrej Gogala, Miklós Sárospataki, and Peter Šima

Insect Science, 2020

Species range expansions are crucial for understanding niche formation and the interaction with t... more Species range expansions are crucial for understanding niche formation and the interaction with the environment. Here, we studied the bumblebee Bombus haematu-rus Kriechbaumer, 1870, a species historically distributed from northern Serbia through northern Iran which has very recently started expanding northwestward into Central Eu-rope without human-mediated dispersal (i.e., it is a natural spread). After updating the global distribution of this species, we investigated if niche shifts took place during this range expansion between newly colonized and historical areas. In addition, we have explored which climatic factors may have favored the natural range expansion of the species. Our results indicated that Bombus haematurus has colonized large territories in 7 Euro-pean countries outside the historical area in the period from the 1980s to 2018, a natural expansion over an area that equals 20% of the historical distribution. In addition, this bumblebee performs generalism in flower visitation and it occurs in different habitats, although a preference for forested areas clearly emerges. The land-use associated with the species in the colonized areas is similar to the historical distribution, indicating that no major niche shifts occurred during the spread. Furthermore, in recently colonized localities, the range expansion was associated with warming temperatures during the winter and also during both queen overwintering and emergence phases. These findings document a case of natural range expansion due to environmental change rather than due to niche shifts, and specifically they suggest that warmer winters could be linked to the process of natural colonization of new areas.

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The spread of Bombus haematurus in Italy and its first DNA barcode reference sequence

Fragmenta Entomologica, 2020

Climate change and human activities are impacting species distribution, and thus, tracking specie... more Climate change and human activities are impacting species distribution, and thus, tracking species movements is a key aspect for their conservation and for understanding their biology. Among the bumblebees that are changing distribution, one of the most striking cases of a fast and natural range expansion is the eastern Mediterranean Bombus haematurus. Here we report the first Italian records of this species, with observations from the N-E Italy at a distance of 332 Km from the edge of the historical distribution. These are the westernmost known occurrences of this species and they are not far from a large series of records in several Central European countries of recent colonization. Here, we also obtained and made publicly available the reference COI barcode sequence of Bombus haematurus and shown that is significantly different from other similar species at this genetic marker. Coupling morphology, field-data and genetic identity should greatly improve the efficiency of tracking species movements and therefore also their knowledge in both recently colonized and historical areas.

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DNA barcoding unveils the first record of Andrena allosa for Italy and unexpected genetic diversity in Andrena praecox (Hymenoptera: Andrenidae

Fragmenta Entomologica, 2020

DNA barcoding is well-known to support morphological species identification and it can be helpful... more DNA barcoding is well-known to support morphological species identification and it can be helpful for unveiling unexpected populations divergence patterns, especially in the context of the impacts on species posed by global change. In this note, we provided the first Italian record of the alpine mining bee Andrena allosa Warncke, 1975, confirmed with DNA barcoding. In addition, genetic identification of a specimen of Andrena praecox (Scopoli 1753) from western Italy pointed to an unexpected intraspecific genetic structuring at COI DNA barcoding region, with sequences from the Italian and the western sector of its global distribution differing 2.22% (p-dist) from populations of the eastern sector. Given the relevance of these records and of the genetic identity of bee populations from Italy, we argue that implementing molecular surveys in bee monitoring would surely contribute to the conservation of these important pollinators.

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Aberrazioni fiorali di Linaria tonzigii Lona

Notiziario Floristico FAB, 2019

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Experimental loss of generalist plants reveals alterations in plant- pollinator interactions and a constrained flexibility of foraging

by PAOLO BIELLA and Jeff Ollerton

Scientific Reports, 2019

Species extinctions undermine ecosystem functioning, with the loss of a small subset of functiona... more Species extinctions undermine ecosystem functioning, with the loss of a small subset of functionally important species having a disproportionate impact. However, little is known about the effects of species loss on plant-pollinator interactions. We addressed this issue in a field experiment by removing the plant species with the highest visitation frequency, then measuring the impact of plant removal on flower visitation, pollinator effectiveness and insect foraging in several sites. Our results show that total visitation decreased exponentially after removing 1-4 most visited plants, suggesting that these plants could benefit co-occurring ones by maintaining high flower visitor abundances. Although we found large variation among plant species, the redistribution of the pollinator guild affected mostly the other plants with high visitor richness. Also, the plant traits mediated the effect of removal on flower visitation; while visitation of plants which had smaller inflorescences and more sugar per flower increased after removal, flower visitors did not switch between flower shapes and visitation decreased mostly in plants visited by many morpho-species of flower visitors. Together, these results suggest that the potential adaptive foraging was constrained by flower traits. Moreover, pollinator effectiveness fluctuated but was not directly linked to changes of flower visitation. In conclusion, it seems that the loss of generalist plants alters plant-pollinator interactions by decreasing pollinator abundance with implications for pollination and insect foraging. Therefore, generalist plants have high conservation value because they sustain the complex pattern of plant-pollinator interactions. Overall community-level dynamics and ecosystem services are often disproportionately affected by a subset of the local species pool 1,2. This core of functionally important species contains, among others, generalists, which play a dominant ecological role within the community as they are often among the most abundant species 3,4 and interact with a majority of other species 5 , mostly by complex facilitation-competition interactions 6. Generalist plants offer floral resources, mostly sugars from nectar and proteins from pollens, to a wide spectrum of pollinators and thus help to sustain those pollinators' populations 7. A generalist plant is typically visited by both generalist pollinators and specialist ones, which provides multiple advantages. Indeed, visitation by a large number of different pollinators increases the chances of having the pollen dispersed 8. In turn, when gener-alist pollinators are foraging in a patch, they can collect resources from a wide range of plants. This strategy could provide nutritional benefits from multiple sources 9,10 , but may also lead to pollination of several plant species because it is believed that generalist pollinators are visiting only a few plant species during each foraging bout 8. Therefore, conservation of abundant generalists may be important, because their persistence can sustain most of the complexity of interactions taking place in a community 11 .

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Foraging strategies are maintained despite workforce reduction: A multidisciplinary survey on the pollen collected by a social pollinator

PLOS ONE, 2019

The way pollinators gather resources may play a key role for buffering their population declines.... more The way pollinators gather resources may play a key role for buffering their population declines. Social pollinators like bumblebees could adjust their foraging after significant workforce reductions to keep provisions to the colony optimal, especially in terms of pollen diversity and quantity. To test what effects a workforce reduction causes on the foraging for pollen, commercially-acquired colonies of the bumblebee Bombus terrestris were allowed to forage in the field and they were experimentally manipulated by removing half the number of workers. For each bumblebee, the pollen pellets were taxonomically identified with DNA metabarcoding of the ITS2 region followed by a statistical filtering based on ROC curves to filter out underrepresented OTUs. Video cameras and network analyses were employed to investigate changes in foraging strategies and behaviour. After filtering out the false-posi-tives, HTS metabarcoding yielded a high plant diversity in the pollen pellets; for plant identity and pollen quantity traits no differences emerged between samples from treated and from control colonies, suggesting that plant choice was influenced mainly by external factors such as the plant phenology. The colonies responded to the removal of 50% of their workers by increasing the foraging activity of the remaining workers, while only negligible changes were found in diet breadth and indices describing the structure of the pollen transport network. Therefore, a consistency in the bumblebees' feeding strategies emerges in the short term despite the lowered workforce.

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Distribution patterns of the cold adapted bumblebee Bombus alpinus in the Alps and hints of an uphill shift (Insecta: Hymenoptera: Apidae)

by PAOLO BIELLA and Pierre Rasmont

Journal of Insect Conservation, 2017

Climate change is threatening species and habitats. Altitudinal shifts uphill and negative popula... more Climate change is threatening species and habitats. Altitudinal shifts uphill and negative population trends are commonly observed in altitude-related taxa. The bumblebee Bombus alpinus (Linnaeus, 1758) has a disjoint distribution restricted to Fennoscandia and the Alps, and is considered threatened. We studied the ecology and distribution of B. alpinus in the Alps, where the endemic subspecies Bombus alpinus helleri Dalla Torre 1882 is found, as a case-model because of its rarity, habitat, and mutual dependence with the ecosystem for pollination and resources. We developed species distribution models including both climatic and habitat variables to obtain the surface suitable for this subspecies and quantified its protected portion. Our analyses indicate that this bumblebee is restricted to the upper altitudes and has a narrow niche mainly related to the presence of glaciers, the cool temperature, a low temperature variation, and a specific range of precipitation. A strong altitudinal shift is also taking place probably due to climate change. After years of no changes in altitudinal distribution, its lowest altitudinal limit has moved up 479 m since the year 1984, while its upper altitudinal limit has remained unchanged. Over half of the suitable area in the Alps is included within protected areas, but conservation has not been planned yet. However, rare species with narrow niche, such as B. alpinus, are highly threatened by climate change. Potential short-term mitigation actions are discussed, including exchange of males between locations and integral protection of prairies in the vicinity of glaciers.

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Network analysis of phenological units to detect important species in plant-pollinator communities: can it inform conservation strategies?

by PAOLO BIELLA and Jeff Ollerton

Community Ecology, 2017

Conservation of species is often focused either only on those that are endangered, or on maximisi... more Conservation of species is often focused either only on those that are endangered, or on maximising the number recorded on species lists. However, species share space and time with others, thus interacting and building frameworks of relationships that can be unravelled by community-level network analysis. It is these relationships that ultimately drive ecosystem function via the transfer of energy and nutrients. However interactions are rarely considered in conservation planning. Network analysis can be used to detect key species (“hubs”) that play an important role in cohesiveness of networks. We applied this approach to plant-pollinator communities on two montane Northern Apennine grasslands, paying special attention to the modules and the identity of hubs. We performed season-wide sampling and then focused the network analyses on time units consistent with plant phenology. After testing for significance of modules, only some modules were found to be significantly segregated from others. Thus, networks were organized around a structured core of modules with a set of companion species that were not organized into compartments. Using a network approach we obtained a list of important plant and pollinator species, including three Network Hubs of utmost importance, and other hubs of particular biogeographical interest. By having a lot of links and high partner diversity, hubs should convey stability to networks. Due to their role in the networks, taking into account such key species when considering the management of sites could help to preserve the greatest number of interactions and thus support many other species.

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Bombus (Alpinobombus) alpinus in the Italian Central Alps (Hymenoptera: Apidae: Bombinae)

Il Naturalista Valtellinese, 2014

Bombus (Alpinobombus) alpinus (Linné, 1754) è stato recentemente trovato in Valle Cedèc, in Valte... more

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Campylomorphus homalisinus (Elateridae): a new species for Lombardy (Italy), with notes on its ecology, distribution and biogeography

Biodiversity Data Journal 2, 2014

Campylomorphus homalisinus has been found on Mt. Lesima (Northern Apennines) and it is the first ... more Campylomorphus homalisinus has been found on Mt. Lesima (Northern Apennines) and it is the first record for the Lombardy region. C. homalisinus is a rare orophilous species: it has a discontinuous chorology that may have been caused by glaciers dynamics during the Pleistocene era. Little is known about the ecology of the species. This record and the expert-based investigation we performed determined that C. homalisinus inhabits shrublands and grasslands, but may also occur in the forests. This survey includes the only record of C. homalisinus foraging on flowers, a behavior that is not rare in the family Elateridae. We hypothesize that adults integrate their diet with flower resources according to a generalist strategy.

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New records of flower-visiting Muscidae (Diptera) from the Ligurian Apennines of Italy [Neufunde von blütenbesuchenden Muscidae (Diptera) aus dem ligurischen Apennin Italiens

by PAOLO BIELLA and Daniele Avesani

Studia Dipterologica, 2015

Nine species of flower-visiting Muscidae found on Mt. Lesima in the Ligurian Apennines are report... more

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Effects of long- and short-term management on the functional structure of meadows through species turnover and intraspecific trait variability

by Conor Redmond and PAOLO BIELLA

Oecologia, 2016

The functional structures of communities respond to environmental changes by both species replace... more The functional structures of communities respond to environmental changes by both species replacement (turnover) and within-species variation (intraspecific trait variability; ITV). Evidence is lacking on the relative importance of these two components, particularly in response to both short- and long-term environmental disturbance. We hypothesized that such short- and long-term perturbations would induce changes in community functional structure primarily via ITV and turnover, respectively. To test this we applied an experimental design across long-term mown and abandoned meadows, with each plot containing a further level of short-term management treatments: mowing, grazing and abandonment. Within each plot, species composition and trait values [height, shoot biomass, and specific leaf area (SLA)] were recorded on up to five individuals per species. Positive covariations between the contribution of species turnover and ITV occurred for height and shoot biomass in response to both short- and long-term management, indicating that species turnover and intraspecific adjustments selected for similar trait values. Positive covariations also occurred for SLA, but only in response to long-term management. The contributions of turnover and ITV changed depending on both the trait and management trajectory. As expected, communities responded to short-term disturbances mostly through changes in intraspecific trait variability, particularly for height and biomass. Interestingly, for SLA they responded to long-term disturbances by both species turnover and intraspecific adjustments. These findings highlight the importance of both ITV and species turnover in adjusting grassland functional trait response to environmental perturbation, and show that the response is trait specific and affected by disturbance regime history.

Books by PAOLO BIELLA

Lista Rossa IUCN delle api italiane minacciate

Comitato Italiano IUCN e Ministero dell’Ambiente e della Tutela del Territorio e del Mare, Roma, 2018

The main objectives of this research are: 1) the creation of an expert network for the evaluation... more The main objectives of this research are: 1) the creation of an expert network for the evaluation of the extinction risk of wild bees species in Italy; 2) the evaluation of the extinction risk for the species potentially at risk; 3) the identification of the main threats and the conservation actions needed to tackle them. The assessments of extinction risk are based on the IUCN Red List Categories and Criteria and the most updated guidelines. The assessments have been carried out in a workshop with taxonomic focus and involving experts covering different regions of Italy and have been evaluated according to the IUCN standards. A total of 151 species of wild bees native to Italy, for which some indication of decline exists, have been included in the evaluation. The populations were evaluated in their Italian area, including large and small islands where necessary. Of the 151 species assessed, 5 are Critically Endangered and have not been recorded recently. For this reason they are classified as Possibly Extinct. Of the remaining species, 2 are Critically Endangered, 10 are Endangered, 4 are Vulnerable. An additional 13 species are Near Threatened, meaning that they are close to one of the three threat categories. The main threats to wild bees are related to land use change (agricultural intensification and expansion, urbanization, but also - for some species - natural reforestation following the abandonment of rural areas and overgrazing). Some species may be sensitive to climate change. The Red List is a fundamental tool for the identification of conservation priorities, but it is not a list of priorities on its own. Other elements instrumental to priority setting include the cost of action, the probability of success, and the proportion of the global population of each species living in Italy, which determines the national responsibility in the long term conservation of that species.

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