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Journal of Applied Entomology, 2024; 0:1–14
https://doi.org/10.1111/jen.13359
1 of 14
Journal of Applied Entomology
REVIEW ARTICLE OPEN ACCESS
The Neglected Pollinators: Understanding the Importance of Lesser-Known Insect Taxa in Pollination
From Stream to Bloom: Exploring the Potential Role of
Aquatic Insects for Pollination in Wetland Environments
CassandreMurail1 | MathildeBaude2,3 | BenjaminBergerot4 | BenoitGeslin4,5 | NicolasLegay1,6 | IreneVillalta7 |
SabineGreulich1
1Interdisciplinary Research Unit CItés, TERritoires, Environnement et Sociétés (CNRS UMR 7324 CITERES), University of Tours, Tours,
France | 2University of Orleans, Chateau de la Source, Orleans Cedex 2, France | 3Sorbonne University, UPEC, University Paris Cité, CNRS, IRD, INRAE,
Institute of Ecology and Environmental Sciences of Paris (iEESParis), Paris, France | 4Ecosystèmes, Biodiversité, Evolution (CNR S UMR 6553 ECOBIO),
University of Rennes, Rennes, France | 5Institut Méditerranéen de la Biodiversité et d'Écologie marine et continentale (CNRS UMR 7263 IMBE), University
of Aix- Marseille, Marseille, France | 6Institut National des Sciences Appliquées (CNRS 7324 INSA) Centre Val de Loire, Blois, France | 7Institut de
Recherche Sur la Biologie de l'Insecte (CNR S UMR 7261 IRBI), University of Tours, Tours, France
Correspondence: Cassandre Murail (cassandre.murail-zimmermann@univ-tours.fr)
Received: 9 July 2024 | Revised: 23 September 2024 | Accepted: 2 October 2024
Funding: This study was funded by the French National Research Agency (ANR) under the STR ANGE (Ecosystem Serv ices provided by sTReams to
AdjaceNt aGricultural tErrestrial ecosystems) project (ANR- 23- CE03- 00 06).
Keywords: aquatic pollinators| aquatic subsidies| plant–pollinator interactions| riparian pollination| riparian vegetation| stream insects| winged
aquatic insects
ABSTRACT
The substantial loss of insects we are experiencing today has been highlighted all over the world. There is a growing concern
about the global decline of pollinators and its impact on terrestrial and agricultural ecosystems, but the focus of scientists towards
bees remains the rule. Therefore, the role of other insect taxa in pollination is still overlooked. Our review focused on some of
these neglected pollinating taxa, the winged aquatic insects, i.e., insects with an aquatic larval stage such as Ephemeroptera,
Trichoptera, Plecoptera (ETP), Megaloptera and some aquatic Diptera. We first documented the visitors of aquatic and wetland
flowering plants, anticipating a greater presence of aquatic insects on these plants compared to terrestrial pollinators. Secondly,
we documented plant visits, pollen found in gut contents and pollen transfers performed by aquatic insects. Our results revealed
a surprisingly low proportion of aquatic insects visiting both aquatic and wetland plants, suggesting a potential gap in the lit-
erature. The scarcity of articles dedicated to pollen transfer by aquatic insects also indicates that they are fewly considered in
ecological studies. While the role of aquatic insects in pollination is not well documented in the literature, records of their f lower
visits and pollen found on them or in their gut contents do exist and are promising clues to consider them as effective pollinators.
Future research is needed to provide new insights into the importance of winged aquatic insects for the reproductive success of
plants, which could also be an argument for the importance of wetland conservation.
1 | Introduction
Decades of research have documented the significant loss of in-
sects we face today (Van Klink etal. 2024). Seibold etal.(2019)
reported a decline of up to 78% in arthropod abundance in
natural areas. Of particular concern are insect pollinators,
which play an essential role in the support of both wild (Aguilar
etal.2006; Ollerton, Winfree, and Tarrant2010) and cultivated
plant communities (Klein etal.2007; Garibaldi etal.2014). But
while interest in pollinators has grown considerably in recent
This is a n open access ar ticle under the terms of t he Creative Commons Attr ibution-NonCommercial-NoDer ivs License, whi ch permits use and d istribution in any me dium, provided th e original
work is properl y cited, the use is non- commercial and no mo difications or a daptations are ma de.
© 2024 T he Author(s). Journal of Applied Entomology published by W iley-VCH GmbH.
2 of 14 Journal of Applied Entomology, 2024
years, att ention is often limited to b ees and their role in the repro-
ductive success of cultivated plants (Smith and Saunders2016;
Valido, Rodríguez- Rodríguez, and Jordano2019).
If the decline of both honeybee s and wild bees is reach ing spectac-
ular levels (Blackburn2012; Bianco, Cooper, and Fournier2014),
other insect taxa such as Lepidoptera, Coleoptera and Diptera
are not less affected (e.g., more than half of the Syrphidae are
threatened according to the IUCN2022). Indeed, they also play
an essential role as they can support pollination services in ag-
ricultural environments (Orford et al. 2016; Rader et al.2015;
Requier et al. 2023). Several studies have also shown that a
greater diversity of pollinators increases the reproductive suc-
cess of plants (Albrecht etal.2012; Schurr etal.2021), and there-
fore, a more advantageous pollination strategy should be based
on as many different species as possible to ensure our food sov-
ereignty. To explore this pollinator diversity, it is interesting to
take a closer look at areas that are known to harbour incredibly
rich biodiversity, such as aquatic and wetland areas (e.g., pond
margins, rivers, streams, ditches and wet grasslands) (Williams
etal.2003; Dudgeon etal.2006). Freshwater eco systems not only
shelter important flowering resources for pollinators (Zhang
etal.2022), they also host 9.5% of the Earth's described animal
species, 60% of which are aquatic insects (Balian et al.2008).
Aquatic and semiaquatic insects can be found in all freshwater
ecosystems (Lancaster and Downes2013), representing almost
100,000 species divided into 12 orders (Dijkstra, Monaghan,
and Pauls2013). Among the aquatic arthropods (i.e., with a lar-
val aquatic stage and a flying adult stage), the Ephemeroptera,
Trichoptera, Plecoptera (abbreviated as ETP), Odonata and
Megaloptera members are the most studied. Other orders such
as Diptera, Lepidoptera or Hemiptera may also include aquatic
species or families (Vallenduuk and Cuppen 2004; Dijkstra,
Monaghan, and Pauls2013). Concerning Diptera, to our knowl-
edge, there is no exhaustive inventory of species with aquatic
larvae, except for Chironomidae, Culicidae and some Syrphidae
such as Eristalis tenax (Bertrand1954; Speight2011).
Recently, it has been recognised that aquatic insects have a
fundamental role in aquatic- to- terrestrial subsidies, in part for
their role in soil fertilisation by exporting nitrogen (Stenroth
etal. 2015) or by the nutritional resource they represent for
predators (Gergs etal.2014). Studies showing their roles into
terrestrial food webs continue to open up new perspectives
on their importance in nonaquatic environments (Lafage
etal. 2019). Little is known about the potential interactions
between winged aquatic insects and flowering plants near wa-
tercourses; however, Raitif, Plantegenest, and Roussel(2019)
have suggested that adult flying imago may provide specific
ecosystem services, including pollination when they perch
on flowers, which opens new perspectives to study them as
pollinators. This role, so far rarely considered, would be all
the more interesting since many aquatic insects are known
to have particularly early emergence periods, which would be
a real asset for the reproduction of early wild and cultivated
plants (Raitif et al. 2022). Given their ubiquity, abundance
and extreme diversity (Lancaster and Downes2013), it seems
thus surprising that aquatic insects do not play a role in pol-
lination. At the same time, preliminary information on the
feeding habits of specific winged aquatic insects suggests that
they are likely to be involved in pollination. Indeed, although
nectar feeding was rarely observed, the mouthparts of certain
Trichoptera (Lectrotarsidae, Kokiriidae and Stenopsychidae)
are known to be adapted to ingest liquid food (Krenn, Plant,
and Szucsich 2005). Similarly, within Plecoptera, adults of
Systellognatha have reduced mouthparts and may ingest nec-
tar, whereas adults of Euholognatha are considered to feed on
flower pollen and nectar (Stewart etal.2016). Ephemeroptera
do not have mouthparts, but this does not mean they cannot
be pollen carriers. Again, there is a notable gap in the litera-
ture on the precise diet of all imago aquatic insects. However,
understanding whether their trophic regime includes pollen
and/or nectar, similar to established pollinators, could be very
informative about their role. In a global context of pollina-
tor decline, it is essential to study the influence of other less
studied but potentially effective pollinators, such as aquatic
flying insects. Furthermore, it is important to emphasise the
urgency of studying these insect taxa, as freshwater environ-
ments are particularly vulnerable to anthropogenic pressures
(Del- Claro and Guillermo2019; Reid etal.2019).
Even though effective pollination is diff icult to demonstrate, a bib-
liographic survey of flowering plants that are visited by aquatic
insects could give a first hint of their pollinator potential. We
might expect them to be common in wetlands where they orig-
inate, because specific aquatic insects can reach extremely high
abundances (e.g., Chironomidae can form swarms of up to several
millions of individuals, Armitage, Cranston, and Pinder1995). To
address the shortcomings identified above, we have reviewed the
visitors of specific aquatic and wetland flowering plants to enrich
this information. In addition, our literature review also aims to ex-
plore all known interactions between winged aquatic insects and
flowering plants, supported by the presence of specific plant and
aquatic insect traits that contribute to the plant–pollinator rela-
tionship (TableS1). To that end, we address two questions:
i. Who are the flower visitors of aquatic and wetland plants,
and what proportion of them are aquatic insects? This
question was addressed with a particular focus on the
flora of mainland France.
ii. Can aquatic insects pollinate flowers? This question was
explored by inventorying the visits and pollen transfers re-
alised by winged aquatic insects on a global scale.
2 | Materials and Methods
2.1 | Literature Search for the Inventory
of Plant- Pollinator Interactions
All insect and plant species names are based on the last pub-
lished Taxref taxonomic reference updated in January 2024 (ver-
sion 17) (Gargominy etal.2022).
2.1.1 | Selection of Aquatic and Wetland Flowering
Plant Species
We first documented all insects visiting aquatic and wetland
flowering plants (herbaceous species) in mainland France.
Corsica was not included in our survey because of its high
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3 of 14
number of endemic species. The selection of plant species was
based on Baseflor (Julve1998), a free, scientifically recognised
database (Tichý etal.2023; Dengler et al.2023) that compiles
phytosociological and plant ecological data for France and that
includes both native and exotic species. We selected therein spe-
cies with Ellenberg moisture indicator values (adapted to France
by Julve) > 5, that is, meso- hygrophilous to intra- aquatic spe-
cies. We withdrew species living in very specific environments
like saline areas or clearly ornamental species with little pres-
ence outside gardens. This led to a total of 619 species. We then
checked in the EUNIS (EUropean Nature Information System)
habitat database for running waters, the littoral zone, and ripar-
ian and gallery woodland that no species cited as characteristic
of these habitats was omitted.
2.1.2 | Selection of Winged Aquatic Insects
To document the visits of aquatic insects to flowers, we focused
our research at a global scale on ETP, Megaloptera, Odonata
and Diptera with an aquatic larval stage. The lack of ecologi-
cal knowledge about Diptera larvae has led us to concentrate
on Chironomidae and Culicidae. As Syrphidae are very com-
mon Diptera, we also added four Eristalis species whose larvae's
aquatic status has been reported in the literature (Speight2011):
Eristalis tenax, Eristalis arbustorum, Eristalis nemorum and
Eristalis rupium.
2.1.3 | Literature Review of Aquatic Insect Visitors
Keywords used in the Web of Science to summarise the in-
sects visiting aquatic and wetland plants, and the visits made
by aquatic insects are listed in Table1. References of interest
mentioned in articles not listed in our initial search were also
included in our survey. The Database of Pollinator Interactions
(DoPI, Balfour etal.2022) was finally used to complete the re-
sults, by checking the interactions given by the database for all
the plant species or aquatic insects selected.
In addition to documenting aquatic insect visits to flowering
plants available information on pollen loads (pollen grains per
insect) and gut content of aquatic species were recorded to learn
more about their pollen consumption. Sampling periods were
also examined to analyse whether any trends emerged between
the abundance of aquatic insects found and a particular period
of the year.
2.2 | Network Analysis
The R bipartite package (Dormann et al. 2009) was used to
build binary networks based on insect occurrences (presence/
absence) to illustrate the relationships between plants and polli-
nators reported in the literature. To observe whether any trends
emerged, the indicators' species degree and nested rank were also
computed. Species degree refers to the sum of links per species,
while nested rank quantifies generality or specialisation by the
rank of a species in a network matrix re- arranged for maximal
nestedness. We used a normalised version of nested rank, rang-
ing from 0 (most generalist) to 1 (most specialist).
Histograms were constructed using the ggplot package
(Wickham 2016) to illustrate the variation in visitor frequency
within orders.
All figures and analyses were produced using R version 4.3.2.
3 | Results
3.1 | Visitors of Aquatic and Wetland Plants
The search for flower visitors gave results for 87 aquatic, semi-
aquatic and hygrophilic plants in continental France, for a total
of 148 articles (Table S2). Sampling periods were not always
specified; however, in general, the surveys were conducted over
several months, and most of them included June (65 articles),
July (78 articles) and August (61 articles).
Of the 87 plant species, 26 were aquatic or semiaquatic, 14 were
introduced, being 8 out of the 14 considered invasive. They were
visited by 410 different insects identified at the species level and
79 identified at the genus level, belonging to 14 different orders
(Figure 1). More than a thousand insect occurrences were re-
corded (1478). A quatic insect s were represented by 4 occurrences
TABLE | Summary of queries used on Web of Science. Only the combinations that produced a result are shown.
Information Queries
Insect visits to wetland and
aquatic flowering plants
(pollinat* OR pollen*) AND (ptarmica* OR aconitum* OR acorus* OR allium* OR
Anacamptis* OR novi* belgii* OR Betonica* OR Bidens* OR Cardamine* OR Chamaenerion*
OR Centaurium* OR Dactylorhiza* OR Eichhornia* OR Filipendula* OR Fritillaria* OR
Ficaria* verna* OR Gentiana* OR Hesperis* OR rivale* OR Heracleum* OR Impatiens* OR
Lotus* OR Lysimachia* OR Myosotis* OR Narthecium* OR Rhinanthus* OR Ranunculus*
OR Scrophularia* OR Urtica* OR Ludwigia* OR Pseudacorus* OR Pulmonaria* OR
Platanthera* OR Stachys* OR myosotis* OR tetralix* OR Hyacinthoides* OR Utricula* OR
Lythrum* OR lychnis* OR aquatica* OR nymphae* OR nelumbo* OR nuphar* OR crispus* OR
Scutellaria* OR eupatorium* OR epilobium* OR palustr* OR Chamerion* OR Cardamine*
OR Menyanthes* OR Symphyotrichum* OR sagittaria* OR silene* dioica* OR tazetta* OR
paludosa* OR rivulare* OR veronica* OR Viburnum* OR Vaccinium* OR Viccia*)
Visits by aquatic insects (Ephem* OR Trichop* OR Plecop* OR Megalo* OR Chirono* OR Odona* OR Culici* OR Eris* tenax*
OR Eris* arbustorum* OR Eris* nemorum* OR Eris* rupium*) AND (pollinat* OR nect* OR pollen*)
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4 of 14 Journal of Applied Entomology, 2024
FIGUR E | Legend on next page.
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5 of 14
of ETP, 5 Odonata and 36 occurrences of Diptera from aquatic
environments (1 Chironomidae, 4 Culicidae and 31 Syrphidae
with aquatic larval stage) (Figure2).
Honeybees aside, the most frequent visitors were all from
the Bombus genus. The plant Heracleum sphondylium was
the most visited with 120 different insect species visits and
highly generalist according to the nested rank (0). Although
Hymenoptera was the most represented order, Diptera was
second with a strong presence of hoverflies. The aquatic
Syrphidae Eristalis tenax is the most generalist aquatic insect
of the review (nested rank: 0.02), followed by E. nemorum
(0.03) and E. arbustorum (0.05).
Water lilies (Nymphoides peltata and Nuphar lutea) were the
most visited plants by aquatic insects (Odonata, Trichoptera and
Diptera) followed by Cirsium palust re, but only visited by aquatic
Syrphidae, being also the second most generalist f lowering plant
of all (nested rank = 0.01) just after Heracleum sphondylium (0).
3.2 | Aquatic Insects Visiting Flowers
Our worldwide aquatic insect survey identified 76 articles and
returned 37 insect taxa that were identified at the species level
and 5 insect taxa identified at the genus level. They were divided
into seven orders, visiting 102 plant taxa identified at the spe-
cies level and 20 at the genus level. Of the plant species visited
by aquatic insects, 7 were aquatic or semi- aquatic according
to the selected Ellenberg's indicator moisture values, 52 were
specific to wetlands and 43 were terrestrial plants (Figure 3,
Table S3). Most of the surveyed aquatic insects were Diptera
(220 occurrences), followed by Plecoptera (17), Trichoptera (7),
Megaloptera (5), Odonata (5) and Ephemeroptera (2).
Sampling periods were not always specified, but
Ephemeroptera, Trichoptera and Megaloptera were mostly
found in the beginning of the summer (six occurrences in June
and six in July), while Plecoptera were found all along the year
with a slight peak in May (four occurrences), and Diptera were
found most in summer (33 occurrences in July, 28 in June and
21 in August).
Of the 76 selected articles, 22 also documented effective pollen
transfers by microscopic analysis (TableS4). The pollen loads
(mean number of pollen grains attached to the insect) were es-
timated in 13 articles for five different species, other aquatic in-
sects having only traces of pollen attached to their body parts
(Table2).
In the literature documenting gut contents, six articles men-
tioned pollen found in the gut contents of six different families of
Plecoptera, one Diptera and one Megaloptera. They were mainly
from trees, especially pines (Table3).
The first most generalist species were all Diptera according
to the nested rank. The lowest values were found for Eristalis
tenax (0), which was found to visit 75 different plant species, and
E. nemor um (0.03), visiting 41 of them.
4 | Discussion
Our results undoubtedly reflect a lack of aquatic insects in the
literature. Two hypotheses could explain this absence: Either
they are not able to pollinate f lowering plants due to morpho-
logical or behavioural constraints, or they are not considered
by researchers while studying pollination. Through a thorough
analysis of our results, we will evaluate both options and try to
understand why there are so few aquatic insects in pollination
studies.
4.1 | A Low Representation of Aquatic Insects
Our review first documented the visits made by 14 differ-
ent insect orders to 87 aquatic and wetland flowering plant
species. Most of the insect orders found have few represen-
tatives, while the main visitors are highly dominated by
Hymenoptera, followed by Diptera, then Lepidoptera and fi-
nally Coleoptera. Our results also underline the importance
of wetlands for providing resources to common pollinators,
as shown by the plant species Heracleum sphondylium that is
highly visited by Bombus sp., or the plant species Lysimachia
vulgaris supporting the monolectic bee Macropis europaea
(Hoffmann2005; Triponez etal.2015). Strange though, of the
148 articles we reviewed, only 22 of them mentioned aquatic
insects, which is surprisingly low regarding the type of docu-
mented habitats.
To gain a deeper understanding of visits made by aquatic in-
sects, the second step of our review examined the records of
aquatic insect visitations on a global scale documented by 76
articles. Most of them focused on the four targeted Syrphidae
species. Excluding this family, only 18 relevant articles were
found. Including articles that focus on the importance of pol-
linators other than bees, aquatic insects other than Eristalis sp.
are barely mentioned, nor is their aquatic ecology at the larval
stage (Rader etal.2020).
The first hypothesis that could explain the absence of aquatic
insects is their inability to pollinate. This assumption would
be rather surprising for two reasons. First, the biomass of
emerging aquatic insects can reach 1200–2500 kg ha−1 year−1
in lakes (Gratton and Vander Zanden 2009; Del- Claro and
Guillermo2019). In agricultural landscapes, 12.5 kg ha−1 year−1
of aquatic insect s also emerge from streams and fa ll to the ground
within 10 m of the stream (Raitif etal.2022). Secondly, aquatic
insects are represented by nearly 100,000 species belonging to
FIGUR E | Bipartite network between insects and aquatic/wetland plants present in France. Left: Plant species. Right: Insect families coloured
according to orders (Hymenoptera: Golden; Diptera: Bluish green; Coleoptera: Green; Lepidoptera: Orange; Orthoptera: Red; Ephemeroptera:
Turquoise; Thysanoptera: Brown; Hemiptera: Beige; Odonata: Blue; Trichoptera: Purple). The four remaining orders (Plecoptera, Dermaptera,
Mecoptera and Neuroptera) have not been documented to the family taxonomic level. Aquatic or semiaquatic families are indicated by blue figures.
See TableS1 for the whole plant species names.
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6 of 14 Journal of Applied Entomology, 2024
12 orders (Dijkstra, Monaghan, and Pauls 2013), so it is highly
unlikely that they would not come into contact with flowers in
aquatic or riparian environments. This suggests that even if the
contact with the flower is accidental, the act of pollination can
still occur.
On the other hand, another hypothesis would justify the
absence of aquatic insects for the simple reason that they
are not considered by researchers. An argument favour-
ing this assumption is that most aquatic insects in the ar-
ticles are not identified to species or even family level
(Smith- Ramírez etal.2005; Manning and Cutler2013). They
are also likely to be classified as ‘other’ in studies, or even set
aside as minor pollinators (Horth, Campbell, and Bray2 014).
Due to the difficulty of identifying many aquatic species, the
lack of ecological information on the aquatic status of their
larvae (such as Diptera) or the lack of information on their
pollination efficiency (Ostrowiecka et al. 2019), it is under-
standable that aquatic insects have long been sidelined. It is
therefore imperative to further investigate to fill this gap, as
aquatic insects are probably much more involved in diverse
ecosystem functions than previously thought.
FIGUR E | Visitor frequency of hygrophilic and aquatic plants.
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7 of 14
FIGUR E | Bipartite network between aquatic insects and visited plants. Left: Plant species. Right: Insect species coloured according to orders
(Diptera: Bluish- green; Ephemeroptera: Turquoise; Plecoptera: Lavender; Trichoptera: Purple; Odonata: Blue; Megaloptera: Pink). See TableS2 for
the whole plant species names.
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8 of 14 Journal of Applied Entomology, 2024
4.2 | Why So Few Aquatic Insects?
4.2.1 | Complex and Multifaceted Ecologies
First of all, few aquatic insects were found in the literature
partly because many of them are poorly known and difficult to
identify. For instance, regarding aquatic Diptera, they extend
beyond Chironomidae and Culicidae, but compiling a compre-
hensive list of all species with aquatic larvae is challenging. For
example, certain hoverflies include species with aquatic larvae,
but many of them require redescription and there is no exhaus-
tive list summarising them, which explains why only a minority
TABLE | Aquatic insects carrying pollen and pollen load (mean number of pollen grains) per insect.
References
Insect
order Insect family Insect species
Pollen
load
Free and Williams(1973)Diptera Syrphidae Eristalis arbustorum 261
Levesque and Burger(1982)Diptera Syrphidae Eristalis tenax 278–318
Petanidou etal.(1995)Diptera Syrphidae Eristalis tenax 597
Gómez & Zamora (1999)Diptera Syrphidae Eristalis tenax 136
Diaz and Kite(2002)Diptera Chironomidae Smittia pratorum 5
Pérez- Bañón etal.(2003)Diptera Syrphidae Eristalis tenax 715
Pérez- Bañón, Petanidou, and Marcos- García(2007)Diptera Syrphidae Eristalis tenax 4353
Rader etal.(2009)Diptera Syrphidae Eristalis tenax 106
Sato and Kato(2017)Plecoptera Taeniopterygidae Strophopteryx nohirae 76
Gervais, Chagnon, and Fournier(2018)Diptera Syrphidae Eristalis tenax 313
Gaffney etal.(2018)Diptera Syrphidae Eristalis tenax 10–999
Sugiura and Miyazaki(2021)Megaloptera Corydalidae Neochauliodes
amamioshimanus
46
Rashid etal.(2023)Diptera Syrphidae Eristalis tenax 2503
TABLE | Pollen found in the gut contents of eight different families of aquatic insects.
Reference Insect family Insect species Host plant family
Zwick(1990), Germany Chloroperlidae (Plecoptera) Siphonoperla sp. Pinaceae
De Figueroa and Sánchez-
Ortega(2000), Spain
Capniidae (Plecoptera) Capnioneura mitis
Leuctridae (Plecoptera) Leuctra andalusiaca
Leuctra fusca
Leuctra iliberis
Leuctra inermis
Leuctra maroccana
Nemouroidae (Plecoptera) Amphinemura triangularis
Nemoura cinerea
Protonemura alcazaba
Protonemura meyeri
Pérez- Bañón etal.(2003), Spain Syrphidae (Diptera) Eristalis tenax Fabaceae (Medicago citrina)
Winterbourn(2005), New- Zeland Notonemouridae
(Plecoptera)
Cristaperla fimbria Fagaceae (Nothofagus sp.)
Spaniocerca zelandica
Winterbourn and Pohe(2017),
New- Zeland
Eustheniidae (Plecoptera) Stenoperla maclellani Podocarpaceae
Stenoperla prasina
Sugiura and Miyazaki(2021),
Japan
Corydalidae (Megaloptera) Neochauliodes amamioshimanus Theaceae (Schima wallichii)
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9 of 14
were included in our study (Speight2011). Additionally, fami-
lies like the Tabanidae lack sufficient information about their
aquatic lifestyle (Bertrand1954), suggesting that the diversity
of aquatic Diptera capable of pollination could be much broader
than currently recognised.
The aquatic phases of ETP, Megaloptera and Odonata are much
better known than that of Diptera. However, there remains a
gap in understanding their ecology during the terrestrial phase.
To our knowledge, the first ETP landscape distribution maps
were only published in 2023 (Gerber etal. 2023). The fact that
these insects are able to play a role in terrestrial environments
during their adult stage, participating in the functioning of
these ecosystems, is only very recent (Raitif, Plantegenest, and
Roussel2019).
The ecology of Odonata is better known for both aquatic and
terrestrial phases (Del- Claro and Guillermo 2019). We re-
ported several Odonata in the course of our survey. Given the
plant species where Odonata have been recorded, with very
large floating flowers (waterlilies), it is likely that dragonf lies
and damself lies just perch on flowers as a support, with no
particular purpose to visit them. In addition, their impact on
pollination is probably more detrimental than beneficial, as
they are known to predate valuable pollinators such as bees
(Knight et al. 2005). In summary, Odonata appear to be less
good candidates for pollination, justifying a more specific
interest in ETP, Megaloptera and Diptera in our following
discussion.
4.2.2 | A Reduced Spatial Range
The limited f light capabilities of most ETP may slightly ex-
plain the lack of consideration for aquatic insects as pollinators.
Distribution modelling of ETP performed by Gerber etal.(2023)
indicates that distance to water is a strong informative vari-
able in their models, such that the aquatic insect abundance
decreases with the distance from the watercourse. Similarly,
Carlson etal.(2016) observed that the abundance of Trichoptera
decreased exponentially with distance from the stream. Raitif
etal.(2022) confirmed that most of the ETP were captured close
to the stream, but certain Ephemeroptera and Trichoptera were
found at several dozen meters. A recent review by Peredo Arce
etal.(2023) however emphasises the great variability in flying
abilities among ETP species and that some of them appear to be
capable of flying several kilometres from the stream.
Aquatic Diptera are considered to have better dispersal ca-
pacities than ETP (e.g., chironomids, Rundle, Bilton, and
Fogo2007) due to their ability to use winds for passive dis-
persal. Muehlbauer etal.(2014) found few ETP more than a
100 m from the stream, but several Chironomidae up to 20 km.
This would be consistent with the fact that our review found
much more aquatic Diptera than other aquatic insects visiting
flowers.
Since riparian zones are not the first areas considered for
pollinator sampling, it is not surprising that ETP are rarely
found in many studies. However, our review of aquatic and
hygrophilic plants should have shown a high number of ETP
visitors, since the surveys took place logically near water-
courses, but this was not the case. It is nevertheless import-
ant to note that in the 76 articles mentioning aquatic insect
visitations, only 7 of the visited flowering plants were aquatic
or semiaquatic, 52 were hygrophilic, while the remaining 43
plants were terrestrial (TableS2). One hypothesis to explain
this observation could be that the ability of aquatic insects
to move away from the stream and even to visit trees (e.g.,
Corylopsis gotoana) has been underestimated, challenging the
assumption of their limited flying abilities. Alternatively, an-
other explanation could be the ability of certain aquatic in-
sects to lay eggs in temporary water reservoirs like puddles
(Frouz, Matěna, and Ali2013; Sohn2007). These intermittent
water sources are often overlooked when assessing the distri-
bution of aquatic insects, potentially leading to an underesti-
mation of their presence in the environment. Indeed, certain
species like, Eristalis tenax and E. arbu storum are able to lay
their eggs elsewhere than in watercourses, like in semiaque-
ous organically rich materials such as manure or compost
(Rader etal. 2020), which can partly explain why they were
much more frequently reported in the surveys than ETP. In
any case, it would be worthwhile to integrate new monitoring
efforts of aquatic insects across variable distances from water-
courses. This approach would allow a more thorough assess-
ment of their dispersal capabilities, not just at the taxonomic
order level but also at the species level. This could help to shed
light on their flying abilities, which are currently inadequately
understood and poorly documented in the scientific literature.
4.2.3 | A Limited Time Window
A third explanation for the scarcity of aquatic insects in the lit-
erature could be the limited emergence time window of the ETP.
According to Raitif et al. (2022), Ephemeroptera emerge only in
spring and Trichoptera in spring and early summer in North tem-
perate regions. Plecoptera being the largest exclusively aquatic
order (Dijkstra, Monaghan, and Pauls 2013), it includes families
with diverse ecologies, some of which exhibit a broader temporal
range of emergence than the other two ETP taxa, including win-
ter (Lancaster and Downes 2013; Cheney et al.2019). Similarly,
Chironomidae, the most widely distributed family with an es-
timated 15,000 species worldwide, can emerge throughout the
year in temperate regions (Armitage, Cranston, and Pinder1995).
Finally, the Eristalis sp. reported in our survey emerge almost all
year long except in winter with E. rupium predominantly emerg-
ing during the summer period (Speight2011).
Thus, with the exception of Diptera and Plecoptera, aquatic insects
generally emerge earlier in the season compared with many pol-
linators. This timing discrepancy may partly explain their lower
representation in surveys, which are usually conducted later in the
season to maximise terrestrial insect abundance. This hypothesis
is supported by our results, as most of the surveys documenting
the floral visitors of aquatic and wetland plants were conducted
in the height of summer (June to August in temperate regions),
corresponding w ith the flowering peak of many plant species. This
timeframe may be slightly late to coincide with the peak activity
of many aquatic insects. Our results however do not clearly show
a strong temporal emergence trend towards spring, but the scarce
literature offers too few articles to draw general conclusions.
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10 of 14 Journal of Applied Entomology, 2024
It is nevertheless worth noting that the early emergence of
aquatic insects could be very beneficial for agrosystems, as they
could pollinate spring cultures such as Brassica napus (among
other services) during periods when common pollinators are
rather absent (Wissinger1995).
4.3 | Functional Role of Aquatic Insects in
Pollination
There is a real lack of scientific knowledge concerning the pol-
lination ability of aquatic insects. Nested rank shows that cer-
tain aquatic insects like Eristalis sp. are highly generalists and
thus able to visit a wide variety of different plant species. This
suggests their significant role in the structure and stability of
plant–pollinator networks of wetland environments (Martin
Gonzalez2010). However, considering a visit as an act of pol-
lination is under debate (King, Ballantyne, and Willmer2013).
Assessing pollen load is an effective method to distinguish be-
tween visitation and pollination, but the information is often
lacking for aquatic insects. For example, pollen loads are some-
times only assessed for specific insect taxa, as in the study by
Walton etal. (2020) which only recorded pollen from moths,
although other insects, including Diptera, were sampled. Hence,
there are only a few aquatic insects for which pollen transfer
has been documented, and these are almost exclusively Diptera.
Although pollen loads vary among f lower species because pollen
grains vary in size and shape, Eristalis sp. appear to carry very
large amounts of pollen. Furthermore, it is often stated in the
literature that Eristalis tenax are incredibly efficient pollinators,
even more than certain Hymenoptera, because of their densely
covered bodies with finely branched hairs, capable of carrying
16–54 times more pollen than unspecialised flies (Levesque and
Burger1982; Talavera etal.2001; Gaffney etal.2018). Moreover,
traces of pollen have also been found on some ETP. Some authors
have even been able to estimate pollen loads for a Plecoptera and
a Megaloptera, which although low, were not insignificant (Sato
and Kato2017; Sugiura and Miyazaki2021).
In addition, a large gap exists in the scientific literature regard-
ing the precise diet of all imago aquatic insects. However, the
ability of aquatic insects (mainly Plecoptera) to ingest pollen
raises the question about their true role as pollinators. It should
yet be noted that the pollen found in their gut content primar-
ily comes from trees, especially pines. Pines are anemophilous
trees that produce pollen in large quantities and disperse it very
effectively in the environment (Tauber 1965). This result does
therefore not necessarily mean that aquatic insects fly to cones
in trees. Either way, the subject deserves further study, as the
revelation of a trophic regime that includes pollen and nectar in
the same way as recognised pollinators could be ver y instructive
on the role of aquatic insects.
4.4 | Limits of the Review
Some biases are unavoidable and can participate in the low
levels of aquatic insects we found in the literature. For exam-
ple, the omnipresence of Apis mellifera in some surveys but
not in others influences the diversity of pollinators found, as
it is now recognised that the honeybee is known to dominate
plant–pollinator networks (Valido, Rodríguez- Rodríguez, and
Jordano 2019) and could eventually compete with aquatic in-
sects for flowering resources (Requier et al. 2024). Also, cer-
tain studies aim to be exhaustive, while others focus only on
specific species (e.g., the specific visitors of Hammarbya palu-
dosa, Tatarenko, Walker, and Dyson2022), which reduces the
diversity of the surveyed visitors. Certain plant species are not
considered as hygrophilous despite being common in ripar-
ian inventories (e.g., Rubus fruticosus, personal observations),
which may have reduced our results. In the same way, very com-
mon hygrophilous species such as Veronica beccabunga are not
included in our results because the literature lacks data on their
visitors. On the contrary, rarer species such as certain orchids
were far more documented, perhaps precisely because their
rarity attracts more research interest (e.g., Epipactis palustris,
Claessens and Kleynen2016; Gnatiuk etal.2023). Finally, even
considering the high diversity of aquatic insects, Diptera largely
dominate these communities, comprising almost half of all
aquatic insects. Thus, Diptera are much more likely to be found
in surveys, perhaps at the expense of other rarer aquatic orders
such as Megaloptera (Dijkstra, Monaghan, and Pauls2013). It
must also be said that if our study was partly focused on con-
tinental France, the relationship between insects and plants in
humid environments should enhance the interest everywhere,
particularly in tropical ecosystems where insects are often un-
derstudied (Crespo- Pérez etal.2020).
Another difficulty is that quite a few articles are focusing on
ETP through the prism of pollination ecosystem services, in-
cluding specific studies carried out in an agricultural context.
Many studies consider aquatic insects only at the larval stage
(and not adult stage) since their larvae are used as bioindicators
to explore the stream water quality (McCafferty1978; Penrose
and Lenat1982; Lenat1984; Muenz etal.2006; Holt etal.2015).
In addition, ETP are also particularly sensitive to pesticides,
both indirectly at the larval stage or directly at the adult stage,
with species loss estimated at up to 42% in streams (Beketov
et al. 2013). This significant impact on their population may
also explain their rarity in surveys. In that respect, Plecoptera
and Ephemeroptera taxa are considered to be more sensitive to
toxic compounds than Trichoptera and far more than Diptera
(Wogram and Liess 2001), which aligns with our findings of a
higher occurrence of Diptera than ETP in our review.
5 | Conclusion
Pollinators have traditionally been reduced to a small group
of insects that deserve to be upgraded in the light of scientific
progress. It is clear that many taxa are still neglected in pollina-
tion studies, including aquatic insects such as Ephemeroptera,
Plecoptera, Trichoptera, Megaloptera and certain Diptera.
Yet, evidence on the presence of pollen on the bodies or in the
gut contents of aquatic insects suggest that they may be more
involved in pollination than currently documented in the liter-
ature. Indeed, if aquatic insects have unequal flight capabilities
and time windows, they could play a real role in the pollination
ecosystem service, perhaps not by their performance, but by
their abundance and diversity; their hitherto neglected benefits
could then be far more compelling than previously imagined.
14390418, 0, Downloaded from https://onlinelibrary.wiley.com/doi/10.1111/jen.13359 by Cochrane France, Wiley Online Library on [24/10/2024]. See the Terms and Conditions (https://onlinelibrary.wiley.com/terms-and-conditions) on Wiley Online Library for rules of use; OA articles are governed by the applicable Creative Commons License
11 of 14
In addition, aquatic ins ects have already been found on crop plants ,
for example, Trichoptera on cultivated pear (Ramzan etal.2016),
Diptera on kiwifruit flowers (Broussard etal.2022; Howlett etal.
2022), carrots (Pérez- Bañón, Petanidou, and Marcos- García2007;
Gaffney etal. 2018) or even colza (Rader et al. 2009). If aquatic
insects can effectively pollinate crops, this would open up very in-
teresting avenues in terms of ecosystem services. Conversely, the
conservation of aquatic areas could be worthwhile not only from
the point of view of aquatic pollinators, but also because hygroph-
ilous plants provide important trophic resources for various guilds
of pollinators, as shown in our results.
In the context of such an alarming decline in flying insect bio-
mass, it is important to thoroughly consider the role of all pol-
linators in our predictive models of pollinator decline, as they
may have been underestimated. Our review focused in part on
France, but a specific assessment of the role of aquatic insects
is essential worldwide, especially as wetlands are under signif-
icant threat. A better understanding of the ecosystem services
provided by aquatic species could raise the importance of wet-
land conservation and ensure that these critical habitats receive
the protection they need.
Author Contributions
Cassandre Murail: conceptualization, data curation, writing – origi-
nal draft, formal analysis. Mathilde Baude: writing – review and ed-
iting, supervision. Benjamin Bergerot: writing – review and editing.
Benoit Geslin: writing – review and editing. Nicolas Legay: writing
– review and editing. Irene Villalta: writing – review and editing, su-
pervision. Sabine Greulich: writing – review and editing, supervision.
Acknowledgements
We wish to thank Christophe Piscart who helped us to find references
and answered all our questions. We also thank LTSER platforms for
both Zones Ateliers Armorique and Loire.
Conflicts of Interest
The authors declare no conflicts of interest.
Data Availability Statement
The dataset are available in a public repository at: https:// doi. org/ 10.
5281/ zenodo. 13935097.
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Supporting Information
Additional supporting information can be found online in the
Supporting Information section.
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