A comprehensive list of all known host plant species utilised by the Meadow Spittlebug (Philaenus spumarius (L.)) is presented, compiled from published and unpublished sources. P. spumarius feeds on 1311 host plants in 631 genera and 117 families. This appears, by a large margin, to be the greatest number of host species exploited by any herbivorous insect. The Asteraceae (222 species) and Rosaceae (110) together account for 25% of all host species. The Fabaceae (76) and Poaceae (73), are nearly tied for third and fourth place and these four families, combined with the Lamiaceae (62), Apiaceae (50), Brassicaceae (43) and Caprifoliaceae (34), comprise about half of all host species. Hosts are concentrated among herbaceous dicots but range from ferns and grasses to shrubs and trees. Philaenus spumarius is an “extreme polyphage”, which appears to have evolved from a monophage ancestor in the past 3.7 to 7.9 million years. It is also the primary European vector of the emerging plant pathogen Xylella fastidiosa. Its vast host range suggests that it has the potential to spread X. fastidiosa among multiple hosts in any environment in which both the spittlebug and bacterium are present. Fully 47.9% of all known hosts were recorded in the Xylella-inspired BRIGIT citizen science P. spumarius host survey, including 358 hosts new to the documentary record, 27.3% of the 1311 total. This is a strong demonstration of the power of organized amateur observers to contribute to scientific knowledge.
Citation: Thompson V, Harkin C, Stewart AJA (2023) The most polyphagous insect herbivore? Host plant associations of the Meadow spittlebug, Philaenus spumarius (L.). PLoS ONE 18(10): e0291734. https://doi.org/10.1371/journal.pone.0291734
Editor: Janice L. Bossart, Southeastern Louisiana University, UNITED STATES
Received: July 4, 2023; Accepted: September 4, 2023; Published: October 4, 2023
Copyright: © 2023 Thompson et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: All relevant data are within the paper.
Funding: The BRIGIT project was funded by UK Research and Innovation (https://www.ukri.org/) through the Strategic Priorities Fund, by a grant from the Biotechnology and Biological Sciences Research Council (https://www.ukri.org/councils/bbsrc/), with support from the UK Department for Environment, Food and Rural Affairs and the Scottish Government to A.J.A.S and C.H. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
The Meadow spittlebug Philaenus spumarius (L.) (Hemiptera: Aphrophoridae) is one of the world’s most widespread and abundant insects (Fig 1). It is also the major European vector of Xylella fastidiosa Wells et al., an emerging bacterial plant pathogen that threatens crops as diverse as grapes, almonds, citrus and olives [1–4]. Despite its importance, the last comprehensive review of P. spumarius host plants is almost 70 years old . Concern with X. fastidiosa has led to a proliferation of recent studies adding new P. spumarius hosts (e.g. [6–11]), including the BRIGIT citizen scientist initiative in Britain that enlisted amateurs to identify P. spumarius host plants .
a) Frothy spittle mass on one of its common host plants, the legume Lotus corniculatus. bird’s-foot trefoil. The nymph is hidden within. b) Spittle foam removed to expose nymph. The dark red dot is its right eye. Note the swollen sucking pump anterior to the eyes. c) Adult P. spumarius. This is the most common of several colour forms. Photographs by Claire Harkin.
The present work has multiple aims. First, we bring together disparate sources in a publicly available, comprehensive, documented compilation of P. spumarius hosts. This will be of use to investigators studying the spread of X. fastidiosa and broader biological phenomena, such as the evolution of xylem feeding insects and the evolution of extreme polyphagy. Second, we analyse the broad patterns of P. spumarius host exploitation, place it in the context of other highly polyphagous insects, and examine the implications of host patterns for X. fastidiosa spread. Third, we suggest some useful guidelines for future surveys of spittlebug host plants. Finally, we assess the efficacy of the BRIGIT project in corroborating existing host records and establishing new ones. We believe this is the first time a citizen science project of this scope has been tested against the historical record.
Philaenus spumarius first became a major subject of study in the late 1940s and early 1950s in the United States and Canada for its role as a serious non-native pest of alfalfa (Medicago sativa) and other forage legumes . From about 1960 to 2010 it was primarily of interest to entomologists and ecologists working on insect population dynamics and energetics [13–16] and to researchers interested in its remarkable colour polymorphism [17–20]. More recently, it has attracted considerable attention from applied entomologists and pest management scientists, after it was shown to be the primary European vector of X. fastidiosa, a pathogen that causes Olive Quick Decline Syndrome (OQDS), which has devastated olive groves in the Apulia region of Italy [1, 21]. This threat, along with the recent association of P. spumarius with Almond leaf scorch disease (ALSD) in the Alicante and Balearic Islands regions of Spain [22, 23], has generated intense research activity focused on the meadow spittlebug, reflected in an exponential recent rise in publications and citations (175 papers and 2,699 citations since 2010; Web of Science, accessed 21 May 2023). Xylella fastidiosa was introduced from the New World to Europe relatively recently . It has now been detected in over 500 plant species, including crops, ornamentals and trees, across many plant families . To predict which agricultural and natural plant species and ecosystems are at risk, it is crucial to understand the host range of the vector.
Information on P. spumarius host plants is scattered across many languages and continents, from the primary scientific literature to amateur entomology publications, agricultural tracts and unpublished sources. Schmidt [25, 26], apparently an amateur, published the earliest extensive host lists in 1914, totaling 137 species, in a German civic booster journal promoting the progress of science and industry. The next major contributions came from Hawaii [27, 28], following the introduction and proliferation of P. spumarius on Big Island in the 1940s. This work was followed shortly by the 1950 publication of 97 California hosts observed by DeLong and Severin  in the course of the first experiments demonstrating that P. spumarius and other spittlebugs can transmit what is now known to be X. fastidiosa. A series of host lists in American PhD theses [30–33] culminated in 1954 in the 383 species compilation of Weaver & King . Metcalf’s encyclopedic catalog of the Aphrophoridae  includes annotated references to host information in P. spumarius publications through 1955, a very useful source of otherwise obscure observations. In 1965 Noury  compiled a list of about 167 hosts from France and Middle and Northern Europe. Halkka et al.  provide a list of 165 hosts based on 1960s field observations in Finland. A 1993 PhD thesis by Booth  includes records of 90 hosts in natural areas in Wales and New Zealand. Jennifer Owen  and Denis Owen  record observing 143 host species in 47 plant families in their late twentieth century English suburban garden, detailed in notes that we recovered from J. Owen’s papers in the Leicester Museum & Art Gallery. More recently, concern over X. fastidiosa has stimulated a golden age of P. spumarius host studies in the Mediterranean region (references below). We have collected, evaluated and distilled these sources and all others available to us into a single, readily accessible summary table in searchable format.
Sources of information
This work is based on the published literature, both formal and informal, host records associated with museum specimens, personal observations, private communications from colleagues, and the BRIGIT citizen science effort carried out in Britain. The first four sources are encompassed in an unpublished world database of spittlebug host plants built and maintained by VT. Ironically, it contains most published host records for most spittlebugs (Hemiptera: Cercopoidea) except for P. spumarius, which was initially exempted from full incorporation because the number of host records was enormous and because there seemed to be little point in recording the hosts of an insect that appeared to feed on almost any available plant. That changed with increasing concern about the role of P. spumarius as a X. fastidiosa vector. Thousands of P. spumarius records have been added, increasing the database from about 5,000 to 9,000 records over the past two years. Even with these additions it is not comprehensive for P. spumarius, missing for example, all of the BRIGIT citizen science records reported here, which are in a separate database maintained by CH and AJAS. The hosts presented here include all known to us as of May 2023.
The BRIGIT project  ran from 2019 to 2021 with the aim of improving surveillance and response capacity for X. fastidiosa should it be introduced into the UK. A key objective of the project was to develop a greater understanding of the distribution and host plant preferences of P. spumarius, identified as the primary vector of the bacterium in Europe . Citizen scientists were encouraged to submit sightings via a national website for natural history observations or a bespoke portal, supported by identification aids on the BRIGIT website.
Sources of ambiguity
Anomalies in Weaver & King.
Prior to this work, Weaver & King’s 1954 compilation  has been the primary source of P. spumarius host records. It originated as a shorter host list in a preceding thesis by King . Ostensibly, it is an amalgam of 26 cited sources, combined with personal observations in Ohio by Weaver and King themselves. We have tracked down and examined all of the original sources cited. This revealed several anomalies. For example, Weaver and King state that all the records in their compilation are for nymphal hosts and go on to say that they omitted the long 1950 California list compiled by DeLong & Severin  because those authors did not distinguish between nymphal and adult hosts. Nevertheless, they still cite four of the 97 hosts reported in that work, while omitting the rest. They list hosts from Osborn’s 1916 work  without reservation, though Osborn too omits information on whether his observations are for nymphs or adults. Unlike Osborn, DeLong & Severin provide dates and locales for their observations. All were made in Alameda County, on the sunnier, warmer side of San Francisco Bay, in April or the first three weeks of May, or in San Francisco, on the foggier, cooler side of the bay, in April, May or the first week of July. In these areas, for the periods in question, most or all P. spumarius individuals are still in the nymphal stage (VT observations), so it may be reasonably inferred that DeLong & Severin observed nymphs for all listed hosts.
Weaver and King also inexplicably omit about two dozen nymphal hosts listed in Teller , while incorporating 33 others. Likewise, their treatment of Marshall  is problematic. They include most of his records, despite the fact that he does not specify life stage, but attribute one host record to him that is not in his work (Rumex acetosa). They also attribute two of Marshall’s records (Pinus strobus and Rumex occidentalis) to Krauss , making it appear that they came from Hawaii rather than New York State. In another oddity, they misattribute a work by Davis  to the authors of a preceding work by Davis & Mitchell  and get the title of the paper by Davis wrong. These mistakes have the look of clerical errors. In the case of Licent , they include three of the hosts listed, but omit three others, perhaps a case of oversight, since the three unlisted hosts are in a different section of a very long treatise.
More disconcertingly, and for no obvious reason, Weaver and King omit 39 hosts out of 85 listed in Schmidt’s second 1914 paper  and misstate the date of that publication as 1915. Given these anomalies and inconsistencies, we have included only hosts that could be corroborated in the original cited works and incorporate, where appropriate, hosts listed in the original sources that Weaver and King omitted. We include the host records Weaver and King report as their own observations.
Sitting records versus host records.
We distinguish among records for nymphal hosts, adult hosts and plants that host both stages. Nymphal host records are unambiguous because nymphs (Fig 1b) cannot produce spittles (Fig 1a) without feeding. Adult records are more problematic. Adult P. spumarius (Fig 1c) are active insects and move about from plant to plant. Unless accompanied by direct observation of feeding in the form of regularly expelled droplets of excreta, adult records may represent “sitting” rather than feeding individuals. This produces inevitable “noise” in adult host records. To minimize this noise, we have omitted instances in which adult host records are clearly unreliable, including those based on single collected specimens. Nevertheless, some of our adult host records are likely in error, or, at a minimum, insecurely documented. On the other hand, there is no doubt that adults do feed on a wide variety of plants. Aside from eggs, P. spumarius does not have an inactive or dormant stage. They must feed to live, and feed in quantity. When there are a lot of adults on a particular plant or when adults associate with multiple individuals of the same plant species, chances are they are feeding. This is particularly true of the many adults found on trees and shrubs in dry climate summers, when plants in the herbaceous understory have browned out for the season [22, 44, 45].
Spittlebug identity in the BRIGIT citizen science data.
The citizen science survey benefitted from the specific character of the British spittlebug fauna. In many other areas there are common spittlebug species frequenting herbaceous dicots that might easily be misidentified for P. spumarius based on observation of spittles alone. This is less the case in Britain, but two British genera, Neophilaenus and Aphrophora, do include spittlebugs that might be mistaken in the spittle stage for P. spumarius if the nymphs themselves are not examined carefully. The four British Neophilaenus species are restricted almost entirely to monocots and can be screened out by eliminating ambiguous records from grasses and sedges. The four Aphrophora species are primarily insects of trees and shrubs, but the nymphs of the most common and widespread species, Aphrophora alni Fallén, also occasionally feed on herbaceous plants. Thus, although the nymphs are distinct, identification based solely on spittles runs the risk of conflating P. spumarius and A. alni. In practice, however, extensive field collections across the UK undertaken during the BRIGIT project found very few A. alni on herbaceous plants; consequently, this risk is judged to be minimal.
Validation of BRIGIT citizen science host plant records adopted a highly conservative approach: 1) all records based on adult P. spumarius were rejected due to the difficulty in distinguishing between sitting and feeding behaviours, as previously described; 2) nymph host records were accepted only where P. spumarius identification could be confirmed via accompanying photographs; 3) host records based on the presence of spittle were attributed to P. spumarius only when the reported host was an herbaceous dicot.
Changing plant taxonomy.
Botanical nomenclature poses additional hurdles. Some of our sources are over 100 years old and plant taxonomy has moved on. Wherever possible, we have updated species names to conform with current usage. Where we encountered nomenclatural ambiguity, we used two sources to determine currently valid names: the Integrated Taxonomic Information System  and Kew Plants of the World Online . We have updated plant family-level taxonomy to be consistent with contemporary usage, following the template of Christenhusz & Byng . This pared down the number of families by about 9%. In many cases, particularly those involving agricultural or popular sources, we had to make reasonable inferences from common names in multiple languages, an endeavor with its own hazards. We are confident that most of our botanical names are correct and up to date, but in a work of this scale, from such diverse sources, some errors are inevitable. We also recognize the possibility that some of the original plant identifications may have been in error, representing another, hopefully small, source of noise in the data.
Criteria for inclusion of records in this compilation
We have included all naturally occurring hosts for which we have found at least one usable record. We exclude records based solely on laboratory experiments. Most records are reported to species level. In instances in which we encountered a mix of records that were generic-only and species-specific for a given genus, we include only species-specific records, to avoid the possibility of double counting. This makes our host number estimates more conservative, as, in all likelihood, some of the excluded generic records represent species distinct from but congeneric to those included. Holopainen & Varis  report that using this criterion decreased their host total for Lygus rugulipennis from 437 to 402, a reduction of 8%. Application of the same criteria to underlying data for the scales Aspidiotis nerii and Hemiberlesia lataninae  reduced the number of species records by about 12.5% in each case. As noted above, we also exclude records of adult hosts based on single specimens.
In cases in which we have multiple records for the same host species, we have given preference in the following order: formal scientific publications (journal articles, books, stand-alone scientific publications), followed by theses and dissertations, followed by more ephemeral Internet sources, followed by unpublished observations by cited observers. Where we have records for multiple geographic areas, we list all areas and cite at least one record for each. For hosts with records for both nymphs and adults, we cite at least one record for each stage. The goal is to keep the list of references for each host species compact, while documenting the known geographical distribution and observed stages for each host. The 358 citizen science host observations new to science are marked ●●●, while those new to the UK are marked ●●, and those confirming earlier local observations are marked ●.
The geographic units chosen for this report include several with natural boundaries. New Zealand (NZ) and Hawaii (HI) represent discrete island areas where P. spumarius has been introduced. The Azores (AZ), where P. spumarius is likely but not certainly recently introduced [51–53] are a special island case, but one with very few host records. In North America, where P. spumarius is introduced, it has a disjunct distribution , divided by the dryer midsection of the continent into discrete eastern (ENA) and western areas (WNA). Britain and Ireland (B&I) represent another natural division. We somewhat arbitrarily divide continental Europe into four areas: Finland and Scandinavia (F&S), Western Europe (WE), Eastern Europe (EE), and the Mediterranean Basin (MED). See the footnotes to Table 1 for the detailed boundaries. A number of Noury’s  listings are from a source covering “Middle and Northern Europe”, a category that does not fit our arbitrary divisions. These records are recorded as M&NE. A few North American references do not specify which section of the continent the records refer to. These are recorded as EorWNA. Although P. spumarius is frequent in Kyrgyzstan  and is reported across Asia to China and Japan (refs. in ), we found only one host record east of European Russia, in Uzbekistan . P. spumarius has been reported once, on strawberries, on the island of Réunion in the Indian Ocean  but, in the absence of later reports, seems not to have become established.
Table 1 lists 1311 species of Philaenus spumarius host plants, by plant family and binomial in alphabetical order within families. It also gives the life stages observed (nymph and/or adult), the geographical area(s) in which the host association was observed, the BRIGIT citizen science observation status (if any), and selected references.
The headline result is that at 1311 species P. spumarius has far more documented host plants than any other herbivorous insect (Table 2). They include ferns, herbs, shrubs, vines and trees, annuals and perennials, grasses and forbs, plants of the tropics, subtropics, temperate and boreal zones, conifers–just about every imaginable kind of vascular plant except those living submerged in aquatic environments. This extraordinary species level diversity is reinforced in the higher order taxonomic diversity, 117 families and 631 genera. Table 3 summarizes the distribution of host species by family for all families represented by 10 or more species.
Note that P. spumarius has far more recorded hosts than any of the comparison species.
Also included are the number of genera for each host family, the percent of host species from that family among all host species, the cumulative percent of all host species going down the ranking, the number of species in each host family, and an index of the occurrence of host species by family weighted for family size. The weighted occurrence index is the number of host species in each family divided by the total number of species in each family and expressed as a percentage. It provides a crude measure of the relative prominence of each host family, taking into account the large differences in numbers of species per family.
A large majority of host records, 1113 (84.9%), are for nymphs only. Eighty-eight (6.7%) are for nymphs and adults, and 6.6% (86) for adults alone (in 24 cases the life stage could not be determined or reasonably inferred from the information available). We include about 1890 geographical area records. Most hosts have been recorded from a single geographical area, but many are recorded from two or more. Multiple area hosts are typically widespread weedy herbs or common garden plants. Europe and North America account for most geographical records, 73.2% and 19.6% respectively, but Hawaii (4.1%) and New Zealand (2.8%) are well represented for their size. Britain and Ireland loom especially large, alone accounting for 37.2% of all records, in major part a reflection of the BRIGIT program. BRIGIT citizen science records include 358 hosts that are not duplicated in preexisting sources, a full 27.3% of all recorded hosts. Another 198 (15.1%) represent records that are new to Britain and Ireland. Seventy-two (5.9%) represent confirmation of hosts recorded for Britain and Ireland in preexisting sources. In total, BRIGIT citizen science records include 628 (47.9%) of the 1311 recorded P. spumarius hosts.
Philaenus spumarius appears to be the most polyphagous insect herbivore
We start by comparing P. spumarius with other insects in terms of the number of host species exploited. At 1311 species, P. spumarius has, to our knowledge, more documented hosts than any other herbivorous insect. For comparison, Table 2 lists some of the serious contenders. Following Normark and Johnson , we limit comparisons to insects that feed directly on plant tissues. This excludes organisms like bees and syrphid flies that feed on pollen and nectar, flies that feed on rotting fruit, and leafcutter ants that attack plants but actually eat fungi that they cultivate on the plant material. None of the comparable insect species for which we have found data approach P. spumarius in number of host species. Hyphantria cunea (Drury), the fall webworm caterpillar weighs in closest, with a bit less than half the P. spumarius host numbers, though the webworm data include an unspecified number of artificial feeding tests , which we omitted in our compilation for P. spumarius. The closest arthropod competitor we have found is an arachnid, the red spider mite, Tetranychus urticae Koch, which is said to have more than 1100 hosts in over 140 plant families . This puts T. urticae at the same order of magnitude as P. spumarius in host species number and substantially greater in host family number, the latter probably due to higher representation of plant families confined to the tropics.
Why is P. spumarius so polyphagous?
Our results substantiate Ossiannilsson’s undocumented 1981 assertion that P. spumarius has more than 1000 hosts , an informed guess that had become embedded in the literature (cf. [4, 54, 212]), despite a lack of supporting evidence. A 1977 statement by Halkka & Mikkola  that there are “nearly 4000 recorded food-plant species” is clearly a typographical error. The documented 1311 species in 117 families put P. spumarius squarely in the category of “extreme polyphage”, defined by Normark & Johnson  as species that feed across more than 20 plant families. Like many extreme polyphages, it is a geographically widespread and invasive pest species, with very high population sizes. However, it does not exhibit other characteristics that Normark & Johnson  associate with extremely polyphagous insects, such as flightless females, larval dispersal, parthenogenesis or partiality to woody plants.
What characteristics have, in fact, contributed to the extraordinarily broad host range? Two factors are probably paramount. The first is xylem sap feeding, a nutritional mode that permits access to a food source that is similar across a wide range of host plants and not chemically defended (refs. in [214, 241]). Xylem feeding apparently permits P. spumarius to feed on almost any plant it can penetrate with its mouth parts. The second factor is wide geographical range and the ability to thrive in climates from Hawaii, just south of the Tropic of Cancer , to within 65 km of the Arctic Circle in Finland . Most or all extreme polyphages have cosmopolitan or invasive distributions .
Among xylem feeding insects, which include spittlebugs, cicadas and one subfamily of leafhoppers, P. spumarius is singular in its occupation of most of the Holarctic plus multiple distant islands. By that standard, other xylem feeders have been modest travelers. In addition to P. spumarius, four other spittlebug species have been introduced from Europe to North America , two others to Hawaii , and one other to New Zealand . Two xylem feeding leafhoppers have been introduced from North America to Europe [218, 219], and three cicada species have hopped from New Zealand’s North Island to South Island ( & C. Simon, personal communication). None have achieved anything approaching the reach of P. spumarius. Perhaps not coincidentally, the other well-documented spittlebug extreme polyphage, Aphrophora alni (Table 2), is among the four other spittlebugs introduced from Europe to North America. It is not clear whether wide distribution is a cause or effect of extreme polyphagy. Each is clearly predisposed to promote the other .
Philaenus spumarius polyphagy seems to be a recent evolutionary development. It is one of a cluster of eight closely related Philaenus species living around the Mediterranean Basin . Five are narrow monophages as nymphs, four feeding exclusively on the lily Asphodelus ramosus L. (or its close relatives A. aestevus or A. microcarpus) and one on Eryngium . Two, P. spumarius and its very closely related sister species Philaenus tesselatus, are broad polyphages, though the extent of polyphagy is much less studied in P. tesselatus [223, 224]. The host status of the eighth species, Philaenus arslani, is uncertain. It has been collected from a modest variety of hosts, including three thistles, Cistus and “diverse shrubs” , all apparently but not explicitly adult hosts.
Maryańska-Nadachowska et al. [221, 225] propose that the line leading to P. spumarius originated from an Asphodelus-feeding ancestor between 7.9 and 3.7 Mya. If so, P. spumarius broke out of the Mediterranean monophage pack and spread to an enormous variety of hosts in a relatively short geological time period, exhibiting what Normark & Johnson  describe as a “niche explosion”. Why? One answer might be the evolution of a more extensive arsenal of gene families involved in digestion, detoxification and transport of xenobiotics, as suggested for the red spider mite , the only arthropod we have found with a comparable host range, and for the green peach aphid  and corn earworm , among the runners up for most polyphagous insect herbivore (Table 2). On the other hand, the fact that xylem feeders encounter so few xenobiotics may make heroic detoxification capacity unnecessary. Ongoing work to sequence the complete P. spumarius genome  should provide data for a comparative analysis of the evolution of feeding versatility-related genes in relationship to niche explosion.
Whether or not accompanied by extensive changes in the food assimilation related genome, the rapid evolution of the P. spumarius line from narrow monophagy to extreme polyphagy may have been facilitated by the feeding ecology of the adults. Asphodelus lilies die back in the Mediterranean summer dry season. Philaenus species dependent on Asphodelus as nymphs move to alternative hosts as adults , typically ectomycorrhizal trees and shrubs , a broadening of host range that may have set the stage for the evolution of polyphagy in the P. spumarius line. Although it has been stated that Mediterranean climate P. spumarius aestivate on these summer hosts [44, 222], there is no evidence for a state of summer torpor or hibernation ( & VT observations in California).
The apparent evolution of an extreme polyphage from monophagic ancestors in a relatively short evolutionary interval is highly unusual. Polyphages are rare among herbivorous insects ([229, 230] and references therein), extreme polyphages even more so . Had it been included in the most recent world survey of insect host plant breadth by Forister et al. , Philaenus spumarius would have been, in the most literal sense, off the charts. It seems to be one of a kind. It is also a clear counterexample to the suggestion that extreme polyphagy is an illusion based on multiple indistinguishable cryptic species feeding on different hosts [204, 226]. Extensive work on mitochondrial haplotype distribution in P. spumarius rules out multiple unrecognized cryptic species, although its mitochondrial lineages are bifurcated into two distinct clades [51, 52, 232] and one study suggested the presence of an unrecognized cryptic species in Anatolia and the Caucasus .
Patterns in host plant usage
Given that P. spumarius seems able and willing to feed on almost any available host, what patterns in host usage can we discern? In sheer species numbers (Table 3) the Asteraceae (222) win hands down, with over twice as many hosts as the runner up Rosaceae (110), followed by the Fabaceae (76) and the Poaceae (73). The latter two high ranking groups merit special comment. Spittlebugs have a demonstrated affinity for nitrogen-fixing hosts, including many Fabaceae  (Fig 1a). In P. spumarius this is reflected in its pest status in legume forage crops in North America. Though it occurs on greater host species numbers in Asteraceae, it achieves highest densities on Fabaceae, up to 1280 nymphs/m2 in on M. sativa . The large numbers of Poaceae hosts (71) are surprising in the other direction. It has long been recognized that P. spumarius favors herbaceous dicots and is relatively rare on grasses . While grasses as a group are not preferred hosts, the present results demonstrate that there are relatively large numbers of grass host species, which contribute markedly to total host diversity, and it is clear that P. spumarius is sometimes locally common on grasses. Booth , for example, found P. spumarius plentiful on grasses at some open sites in New Zealand and shaded sites in Wales, while Lester et al.  found P. spumarius to be relatively common on grasses during the Scottish professional BRIGIT survey.
At the high end of the host spectrum, P. spumarius is found not only on large numbers of Asteraceae species, but occurs in large numbers and high density on some individual species, including several Solidago spp. and a number of thistles. Among the Rosaceae, Filipendula ulmaria by itself accounted for 22% of 40,737 nymphal host records collected by Halkka and his colleagues in Finland . This highlights a major limitation of species lists as a measure of host diversity. They count occurrence but not frequency, though local frequency is often recorded in the underlying sources.
Another way to look at host attraction is to compare the ratio of P. spumarius hosts in a given family to the total number of species in that family. Table 3 includes a weighted occurrence index, the percentage of P. spumarius host species among all species in a plant family. This corrects, in a rough and ready way, for the fact that some plant families are small and some are enormous. Given that P. spumarius has an essentially temperate distribution, however, it should be noted that the index will be highly conservative for plant families that have a large proportion of species in the tropics. Among families with at least ten P. spumarius hosts, the index ranges from a low of 0.12 for Rubiaceae to a high of 7.19 for Betulaceae. In relation to total species numbers, P. spumarius occurs on a small proportion of Rubiaceae and a high proportion of Betulaceae. The Pinaceae (4.82), Caprifoliaceae (4.00), Rosaceae (3.42) and Onagraceae (3.05) are also high scoring. In contrast, two of the top three host families, Asteraceae (0.86) and Fabaceae (0.38), are knocked out of this competition by their enormous species numbers. The high rankings of two families comprised solely of trees and shrubs, Betulaceae and Pinaceae, might seem counterintuitive for an insect that clearly favors herbs, but both groups are ectomycorrhizal and their high scores are consistent with the general overrepresentation of this category among spittlebug hosts .
Plant morphology also clearly plays an important role in host plant selection. Early instar nymphs are especially attracted to plants with rosette form or other forms of growth that favor closely apposed leaf surfaces , no doubt because compact leafy clusters in close proximity to soil moisture form an advantageous early-instar nymphal microhabitat. Later instars tend to favor tall and robust perennial herbs . On the other hand, plant features like abundant trichomes and lignification of tissues clearly deter P. spumarius feeding [90, 235]. When P. spumarius nymphs feed on woody plants it is invariably on new, unlignified growth, such as saplings, adventitious shoots of trees, or growing areas at the tips of branches ([5, 121] and our observations).
Are there any otherwise apparently suitable plants on which P. spumarius does not feed? The most intriguing possibility is crownvetch, Coronilla varia L. (synonym Securigera varia (L.) Lassen), a Eurasian legume widely planted for forage and roadside erosion control in Eastern North America. Wheeler  reports that he found P. spumarius “in small numbers as adults only” on crownvetch but excludes it from his extensive list of arthropods collected on crownvetch in Pennsylvania. He adds that F.V. Grau, the founder of crownvetch studies in the USA, reported that he had never seen spittlebugs on this species in 28 years of work. We found no other records for crownvetch, a particularly unexpected result because C. varia is a nitrogen-fixing forage legume, the category of host on which P. spumarius otherwise reaches greatest densities in the USA. This suggests, subject to experimental verification, that there may be something exceptional about its biology that repels P. spumarius. If so, it might be a candidate species for understory plantings in orchards and groves where there is a desire to suppress P. spumarius vector populations .
It also appears that P. spumarius nymphs may not occur on Asclepias, species of which are notoriously well-defended chemically. Beirne  reports that P. spumarius nymphs do not feed on Asclepias species and the only P. spumarius Asclepias record we have found is for adults in Maryland (Table 1). There are, however, Asclepias nymphal records for two Lepyronia species [126, 238], demonstrating that this genus is not off-limits to all spittlebugs. Schmidt  says that he never observed spittles on Chenopodium or Atriplex. Chenopodium album, the species to which he is most likely referring, has been widely recorded as a P. spumarius host, both nymphal and adult, but Atriplex has only been observed as a host once, and only for adults (Table 1), suggesting that this genus may not be hospitable to nymphs. In general, our results sustain the early observations of Schmidt  and Fabre  that nymphs feed successfully on many plants that are chemically well-defended.
Although P. spumarius has been recorded on several fern species (Table 1), it has not been recorded on bryophytes. Press and Whittaker  illustrate a spittle of the grass-feeding spittlebug Neophilaenus lineatus on a moss (Polytrichum commune), demonstrating that mosses are within the realm of plausible hosts. Notable plant categories on which P. spumarius records are rare in relationship to their numbers are Orchidaceae, Bromeliaceae, and CAM plants as a group. This is not surprising for orchids and bromeliads, the large majority of which are tropical epiphytes, putting them largely out of the geographical and ecological range of P. spumarius. It is more surprising for CAM plants, many in the Crassulaceae (eight species in Table 1), which are diverse and widely distributed in areas and habitats that P. spumarius frequents. CAM plants (which overlap to include many species in the Orchidaceae and Bromeliaceae) maintain close control of daytime transpiration, perhaps interfering with the accessibility of xylem sap.
Implications for Xylella fastidiosa management
The most important lesson to be drawn from this review is that P. spumarius can and does feed on an extremely diverse array of plants, including, it appears, almost any vascular plant that comes its way with sufficiently accessible xylem vessels, the only apparent exceptions being, as noted above, Coronilla varia and Asclepius species. Philaenus spumarius nymphs are relatively sessile, moving infrequently, if at all, among hosts. By analogy with their leafhopper vector counterparts , they probably lose any X. fastidiosa infection upon molting, which occurs five times during nymphal development. In consequence, nymphs are not effective vectors. In contrast, adults are known to be effective vectors  but their exact host range is much less certain, with many fewer hosts documented (Table 1), this in turn being substantially due to the difficulty noted in distinguishing between a functional host plant and one on which the insect is merely positioned. Although efficacy of transmission varies greatly with host species , P. spumarius adults are exceptionally well positioned to vector X. fastidiosa quickly and widely wherever the two co-occur, contingent on local conditions that favor the propagation of the bacterium within and among host plants [22, 40, 106]. Potential counter measures include: 1) local elimination or population reduction of P. spumarius by management of agriculturally adjacent host plants [2, 106, 212, 237], 2) reduction or elimination of plant sources of Xylella fastidiosa infection , and 3) reduction of target plant susceptibility, through selection of cultivars with genetic resistance or other measures that reduce plant vulnerability to transmission and/or infection [2, 21, 241, 242]. In turn, P. spumarius can be used as a sentinel organism to detect and monitor the presence of X. fastidiosa in local environments .
Going forward, we suggest several guidelines for future studies of P. spumarius on host plants. First and foremost, investigators should always specify life stage. A substantial number of past reports, especially from the agricultural sector, have omitted this important information. Second, to the degree possible, quantify the results. Counts are best, but even simple qualitative observations, such as “rare” or “abundant” are helpful, especially for observations on adults. Third, where P. spumarius nymphs are abundant, record the plants on which they are apparently absent, especially in instances in which the uninfested plant species are frequent and apparently suitable for feeding. This will assist in the ongoing search for alternative understory plants suitable for reducing P. spumarius numbers in agricultural settings. Recent screening of nymphs in the Basilicata Region of Italy by Trotta et al.  is a model for this approach. The authors include data on 48 plant species that hosted nymphs and on 17 species that did not.
Lessons from the BRIGIT citizen scientist project
Mass-participation citizen science projects have a well-established history of contributing environmental and ecological data over numerical, spatial and temporal scales that would be impossible to collect by professional researchers alone [244, 245]. Concerns about the quality of such data  are counterbalanced by recent studies indicating that the reliability of citizen science data can be significantly enhanced by training, data validation and ground-truthing [247, 248].
The BRIGIT citizen science project proved to be a powerful tool for the rapid collection of large amounts of P. spumarius host plant usage data across the UK. Spittle was found to be a reliable focus for citizen science activity, being highly visible during the nymphal season and largely unmistakable for any other natural phenomena. At least in the UK, therefore, spittle on herbaceous dicots could be used for rapid assessment of both the presence and relative abundance of P. spumarius. Such estimates could form part of a future surveillance strategy for X. fastidiosa, although many other factors would need to be considered when assessing the risk of bacterial transmission.
Finally, we note that the BRIGIT project is the latest installment in a long history of amateur contributions to P. spumarius host records, including the major works of Hugo Schmidt [25, 26], Ernest Noury  and Jennifer Owen . In that sense, the work reported here is a monument to synergism between professional scientists and dedicated amateurs in the advancement of knowledge.
We dedicate this paper to our departed colleagues Olli Halkka and David Lees, and to John Whittaker, pioneers in evolutionary and ecological studies of P. spumarius and other spittlebugs. We thank librarians Mary Beth Riedner (Roosevelt University, retired), Gwen Short (Ohio State University) and Mai Reitmeyer (American Museum of Natural History) for tracking down some of the more obscure and hard-to-access references necessary for a review of this kind. Adeline Soulier-Perkins (Museum National d’Histoire Naturelle) provided a hard-to-find copy of Noury’s host compendium . Martin Harvey (UK Biological Records Centre), Kirsty Gamble (Leicestershire and Rutland Environmental Records Centre) and Alison Clague (Leicester County Council) helped us track down Jennifer Owen’s archived host records. Chris Simon (University of Connecticut) provided unpublished information on New Zealand cicada introductions. Benjamin Normark (University of Massachusetts, Amherst) provided helpful insights and leads on extreme polyphages. Numerous colleagues over the years have shared unpublished host observations, a handful used here and all valuable to the host tracking effort. The BRIGIT project was funded by UK Research and Innovation through the Strategic Priorities Fund, by a grant from the Biotechnology and Biological Sciences Research Council, with support from the UK Department for Environment, Food and Rural Affairs and the Scottish Government, to AJAS and CH. We thank Saskia Hogenhout, Sam Mugford, Roberto Biello and Qun Liu (John Innes Centre, UK) for providing the worldwide host plant records collected during the BRIGIT project.
- 1. Bodino DN, Cavalieri DV, Dongiovanni DC, Saponari DM, Bosco PD. Bioecological traits of spittlebugs and their implications on the epidemiology and control of Xylella fastidiosa epidemic in Apulia (Southern Italy). Phytopathology. 2023. pmid:36945728
- 2. Cornara D, Bosco D, Fereres A. Philaenus spumarius: when an old acquaintance becomes a new threat to European agriculture. J Pest Sci. 2018;91: 957–972.
- 3. Sicard A, Zeilinger AR, Vanhove M, Schartel TE, Beal DJ, Daugherty MP, et al. Xylella fastidiosa: insights into an emerging plant pathogen. Annu Rev Phytopathol. 2018;56: 181–202. pmid:29889627
- 4. Trkulja V, Tomić A, Iličić R, Nožinić M, Milovanović TP. Xylella fastidiosa in Europe: from the introduction to the current status. Plant Pathol J. 2022;38: 551–571. pmid:36503185
- 5. Weaver CR, King DR. Meadow spittlebug, Philaenus leucophthalmus (L.). Research Bulletin 741. Ohio Agricutural Experiment Station, Wooster, Ohio; 1954.
- 6. Antonatos S, Papachristos DP, Kapantaidaki DE, Lytra IC, Varikou K, Evangelou VI, et al. Presence of Cicadomorpha in olive orchards of Greece with special reference to Xylella fastidiosa vectors. J Appl Entomol. 2021;144: 1–11.
- 7. Morente M, Cornara D, Plaza M, Durán JM, Capiscol C, Trillo R, et al. Distribution and relative abundance of insect vectors of Xylella fastidiosa in olive groves of the Iberian peninsula. Insects. 2018;9: 175. pmid:30513710
- 8. Dongiovanni C, Cavalieri V, Bodino N, Tauro D, Di Carolo M, Fumarola G, et al. Plant selection and population trend of spittlebug immatures (Hemiptera: Aphrophoridae) in olive groves of the Apulia region of Italy. J Econ Entomol. 2019;112: 67–74. pmid:30265319
- 9. Latini A, Foxi C, Borfecchia F, Lentini A, De Cecco L, Iantosca D, et al. Tacking the vector of Xylella fastidiosa: geo-statistical analysis of long-term field observations on host plants influencing the distribution of Phylaenus [sic] spumarius nymphs. Environ Sci Pollut Res. 2019;26: 6503–6516. pmid:30627995
- 10. Bodino N, Cavalieri V, Dongiovanni C, Saladini MA, Simonetto A, Volani S, et al. Spittlebugs of Mediterranean olive groves: host-plant exploitation throughout the year. Insects. 2020;11: 130. pmid:32085449
- 11. Trotta V, Forlano P, Caccavo V, Fanti P, Battaglia D. A survey of potential vectors of the plant pathogenic bacterium Xylella fastidiosa in the Basilicata Region, Italy. Bull Insectology. 2021;74: 273–283.
- 12. BRIGIT; Surveillance and response capacity for Xylella fastidiosa. In: John Innes Centre [Internet]. [cited 26 May 2023]. https://www.jic.ac.uk/brigit/
- 13. Karban R, Strauss SY. Physiological tolerance, climate change, and a northward range shift in the spittlebug, Philaenus spumarius. Ecol Entomol. 2004;29: 251–254.
- 14. Wiegert RG. Population energetics of meadow spittlebugs (Philaenus spumarius L.) as affected by migration and habitat. Ecol Monogr. 1964;34: 218–241.
- 15. Whittaker JB. Studies on the Auchenorrhyncha (Hemiptera–Insecta) of Pennine moorland with special reference to the Cercopidae. PhD Thesis, Durham University. 1963.
- 16. Masters GJ, Brown VK, Clarke IP, Whittaker JB, Hollier JA. Direct and indirect effects of climate change on insect herbivores: Auchenorrhyncha (Homoptera). Ecol Entomol. 1998;23: 45–52.
- 17. Stewart AJA, Lees DR. The colour/pattern polymorphism of Philaenus spumarius (L.) (Homoptera: Cercopidae) in England and Wales. Philos Trans R Soc Lond B Biol Sci. 1996;351: 69–89.
- 18. Thompson V. Distributional evidence for thermal melanic color forms in Philaenus spumarius, the polymorphic spittlebug. Am Midl Nat. 1984; 288–295.
- 19. Stewart AJA, Lees DR. Genetic control of colour/pattern polymorphism in British populations of the spittlebug Philaenus spumarius (L.) (Homoptera: Aphrophoridae). Biol J Linn Soc. 1988;34: 57–79.
- 20. Thompson V. Parallel colour form distributions in European and North American populations of the spittlebug Philaenus spumarius (L.). J Biogeogr. 1988; 507–512.
- 21. Saponari M, Giampetruzzi A, Loconsole G, Boscia D, Saldarelli P. Xylella fastidiosa in olive in Apulia: Where we stand. Phytopathology. 2019;109: 175–186. pmid:30376439
- 22. Olmo D, Nieto A, Borràs D, Montesinos M, Adrover F, Pascual A, et al. Landscape Epidemiology of Xylella fastidiosa in the Balearic Islands. Agronomy. 2021;11: 473.
- 23. Moralejo E, Gomila M, Montesinos M, Borràs D, Pascual A, Nieto A, et al. Phylogenetic inference enables reconstruction of a long-overlooked outbreak of almond leaf scorch disease (Xylella fastidiosa) in Europe. Commun Biol. 2020;3: 1–13. pmid:33037293
- 24. EFSA EFS, Delbianco A, Gibin D, Pasinato L, Boscia D, Morelli M. Update of the Xylella spp. host plant database–systematic literature search up to 31 December 2021. EFSA J. 2022;20: e07356. pmid:35734284
- 25. Schmidt H. Weitere Bemerkungen zu “die Larve der Schaumzikade (Aphrophora spumaria L.) als gallenbildendes Tier.” Prometheus Leipz. 1914;26: 90–92.
- 26. Schmidt H. Die Larve der Schaumzikade (Aphrophora spumaria L.) als gallenbildendes Tier. Prometheus Leipz. 1914;25: 250–252.
- 27. Davis CJ. Additional hosts of Philaenus spumarius (L.). Proc Hawaii Entomol Soc. 1947;13: 30–31.
- 28. Davis CJ, Mitchell AL. Host records of Philaenus spumarius (Linn.) at Kilauea, Hawaii National Park (Homoptera: Cercopidae). Proc Hawaii Entomol Soc. 1946;12.
- 29. DeLong DM, Severin HHP. Spittle-insect vectors of Pierce’s disease virus. I. Characters, distribution, and food plants. Hilgardia. 1950;19: 339–356.
- 30. King DR. Ecology of the Meadow Spittlebug Philaenus leucophthalmus (L.); Family Cercopidae. PhD thesis, The Ohio State University. 1952.
- 31. Ahmed DD. Life History and Control of the Meadow Spittlebug Philaenus leucophthalmus (Linn.)(Homoptera, Cercopidae). PhD thesis, The Ohio State University. 1949.
- 32. Teller LW. The Meadow Spittlebug, Philaenus leucophthalmus (L.) in Maryland. PhD Thesis, University of Maryland. 1951.
- 33. Marshall DS. The control of the meadow spittlebug (Philaenus leucophthalmus (L.)). PhD Thesis, Cornell University. 1951.
- 34. Metcalf ZP. General Catalogue of the Homoptera. Fascicle VII. Cercopoidea. Part 3. Aphrophoridae. Waverly Press, Baltimore; 1962.
- 35. Noury EM. Les plantes-hôtes de la cicadelle Philaenus spumarius (L.). Cah Nat Bull Nat Paris Ns. 1965;21: 93–97.
- 36. Halkka O, Raatikainen M, Vasarainen A, Heinonen L. Ecology and ecological genetics of Philaenus spumarius (L.) (Homoptera). Ann Zool Fenn. 1967;4: 1–18.
- 37. Booth WJ. Aspects of Host Plant Relationships in Cercopidae (Homoptera: Auchenorrhyncha). PhD thesis, University of Wales, College of Cardiff. 1993.
- 38. Owen J. Wildlife of a Garden: A Thirty-Year Study. Royal Horticultural Society; 2010.
- 39. Owen DF. (1988) Native and alien plants in the diet of Philaenus spumarius (L.) (Homoptera: Cercopidae). Entomol Gaz. 1988;39: 327–328.
- 40. Bodino N, Demichelis S, Simonetto A, Volani S, Saladini MA, Gilioli G, et al. Phenology, seasonal abundance, and host-plant association of spittlebugs (Hemiptera: Aphrophoridae) in vineyards of northwestern Italy. Insects. 2021;12: 1012. pmid:34821812
- 41. Osborn H. Studies of Life Histories of Froghoppers of Maine. Bulletin 254. Maine Agricultural Experiment Station; 1916.
- 42. Krauss NLH. Philaenus spumarius (Linn.). Proc Hawaii Entomol Soc. 1945;12: 220.
- 43. Licent PÉ. Recherches d’anatomie et de physiologie comparées sur le tube digestif des homoptères supérieurs. La Cellule. 1912;28: 1–161.
- 44. Drosopoulos S. New data on the nature and origin of colour polymorphism in the spittlebug genus Philaenus (Hemiptera: Aphrophoridae). Ann Société Entomol Fr NS. 2003;39: 31–42.
- 45. Cornara D, Panzarino O, Santoiemma G, Bodino N, Loverre P, Mastronardi MG, et al. Natural areas as reservoir of candidate vectors of Xylella fastidiosa. Bull Insectology. 2021;74: 173–180.
- 46. ITIS. Integrated Taxonomic Information System. www.itis.gov. 2023.
- 47. PoWO. Plants of the World Online. http://www.plantsoftheworldonline.org/. 2023.
- 48. Christenhusz MJM, Byng JW. The number of known plants species in the world and its annual increase. Phytotaxa. 2016;261: 201–217.
- 49. Holopainen JK, Varis A-L. Host plants of the European tarnished plant bug Lygus rugulipennis Poppius (Het., Miridae). J Appl Entomol. 1991;111: 484–498.
- 50. García Morales M, Denno BD, Miller DR, Miller GL, Ben-Dov Y, Hardy NB. ScaleNet: A literature-based model of scale insect biology and systematics. Database. http://scalenet.info. 2016. pmid:26861659
- 51. Seabra SG, Rodrigues ASB, Silva SE, Neto AC, Pina-Martins F, Marabuto E, et al. Population structure, adaptation and divergence of the meadow spittlebug, Philaenus spumarius (Hemiptera, Aphrophoridae), revealed by genomic and morphological data. PeerJ. 2021;9: e11425. pmid:34131518
- 52. Rodrigues AS, Silva SE, Marabuto E, Silva DN, Wilson MR, Thompson V, et al. New mitochondrial and nuclear evidences support recent demographic expansion and an atypical phylogeographic pattern in the spittlebug Philaenus spumarius (Hemiptera, Aphrophoridae). PLoS One. 2014;9: e98375.
- 53. Borges PAV, Gaspar C, Crespo LCF, Rigal F, Cardoso P, Pereira F, et al. New records and detailed distribution and abundance of selected arthropod species collected between 1999 and 2011 in Azorean native forests. Biodivers Data J. 2016; e10948. pmid:28174509
- 54. Thompson V. Spittlebugs. Ed. by Lamp W.L. et al. Handbook of Forage and Rangeland Insects. Lanham, Maryland: Entomological Society of America; 2007. pp. 91–95.
- 55. Novikov DV, Novikova NV, Anufriev GA, Dietrich CH. Auchenorrhyncha (Hemiptera) of Kyrgyz grasslands. Russ Entomol J. 2006;15: 303–310.
- 56. Kozhevnikova AG. Monitoring of sucking pests of vegetable crops from the (Auchenorrhyncha) series of Uzbekistan. Am J Agric Biomed Eng. 2021;3: 1–5.
- 57. Quilici S, Reynaud B, Bonfils J. Sur deux espèces d’Hémiptères Auchénorrhynques, nouvelles pour la Réunion et d’importance économique potentielle. Bull Société Entomol Fr. 1998 [cited 26 Oct 2022]. https://agritrop.cirad.fr/401125/
- 58. Putman WL. Notes on the bionomics of some Ontario cercopids (Homoptera). Can Entomol. 1953;85: 244–248.
- 59. Thompson V. A new spittlebug of the genus Aphrophora Germar, 1821 (Hemiptera: Cercopoidea: Aphrophoridae) abundant on invasive iceplant, Carpobrotus edulis (L.) N. E. Brown (Aizoaceae), in coastal California. Pan-Pac Entomol. 2021;97: 105–128.
- 60. Rodríguez J, Thompson V, Rubido-Bará M, Cordero-Rivera A, González L. Herbivore accumulation on invasive alien plants increases the distribution range of generalist herbivorous insects and supports proliferation of non-native insect pests. Biol Invasions. 2019;21: 1511–1527.
- 61. Tothova M, Toth P, Cagáň Ľ. Leafhoppers, planthoppers, froghoppers and cixiids (Auchenorrhyncha) on pigweeds as vectors of plant diseases. Acta Fytotech Zootech. 2004;7: 322–326.
- 62. Yildirim E, Özbek H. Insect fauna of sugar beet in sugar beet growing areas of Erzurum Sugar Factory. Proceedings of the Second Turkish National Congress of Entomology. Adana, Turkey; 1992. pp. 621–635.
- 63. Whittaker JB. Polymorphism of Philaenus spumarius (L.) (Homoptera, Cercopidae) in England. J Anim Ecol. 1968;37: 99–111.
- 64. Thanou ZN, Kontogiannis EG, Tsagkarakis AE. Impact of weeds on Auchenorrhyncha incidence and species richness in citrus orchards. Phytoparasitica. 2021;49: 333–347.
- 65. Beirne BP. Pest Insects of Annual Crop Plants in Canada: IV. Hemiptera-Homoptera, V. Orthoptera, VI. Other Groups. Entomological Society of Canada; 1972.
- 66. Blanton FS. Leafhoppers and Homoptera of related families collected in and adjacent to narcissus plantings.1937;30:972. J Econ Entomol. 1937;30: 972.
- 67. Löcker H. Arborikole Zikaden-Gilden in Slowenien:(Hemiptera, Auchenorrhyncha). Cicadina. 2003;6: 7–38.
- 68. Bodino N, Cavalieri V, Dongiovanni C, Plazio E, Saladini MA, Volani S, et al. Phenology, seasonal abundance and stage-structure of spittlebug (Hemiptera: Aphrophoridae) populations in olive groves in Italy. Sci Rep. 2019;9: 17725. pmid:31776426
- 69. Albre J, Carrasco JMG, Gibernau M. Ecology of the meadow spittlebug Philaenus spumarius in the Ajaccio region (Corsica)–I: Spring. Bull Entomol Res. 2021;111: 246–256. pmid:33355061
- 70. Larivière M-C, Fletcher MJ, Larochelle A. Auchenorrhyncha (Insecta: Hemiptera): catalogue. Fauna N Z. 2010;63.
- 71. Kaygin AT, Sönmezyildiz H, Ulgentürk S, Ozdemir I. Insect species damage on ornamental plants and saplings of Bartin Province and its vicinity in the western Black Sea region of Turkey. Int J Mol Sci. 2008;9: 526–541. pmid:19325767
- 72. Nickel H. The Leafhoppers and Planthoppers of Germany (Hemiptera, Auchenorrhyncha): Patterns and Strategies in a Highly Diverse Group of Phytophagous Insects. Sofia: Pensoft Publishers,; 2003.
- 73. Malykh YN, Krisch B, Gerardy-Schahn R, Lapina EB, Shaw L, Schauer R. The presence of N-acetylneuraminic acid in Malpighian tubules of larvae of the cicada Philaenus spumarius. Glycoconj J. 1999;16: 731–739. pmid:11003558
- 74. Lodos N, Kalkandelen A. Preliminary list of Auchenorrhyncha with notes on distribution and importance of species in Turkey. VI. Families Cercopidae and Membracidae. Türkiye Bitki Koruma Derg. 1981;5: 133–149.
- 75. Kaygın AT, Ekİcİ B. Host diversity of Philaenus spumarius (L.) (Hemiptera: Cercopidae) in Bartın Region. Türkiye Entomoloji Bül. 2017;7: 7–13.
- 76. Archibald RD, Cox JM, Deitz LL. New records of plant pests in New Zealand. N Z J Agric Res. 1979;22: 201–207.
- 77. Dáder B, Viñuela E, Moreno A, Plaza M, Garzo E, del Estal P, et al. Sulfoxaflor and natural pyrethrin with piperonyl butoxide are effective alternatives to neonicotinoids against juveniles of Philaenus spumarius, the European vector of Xylella fastidiosa. Insects. 2019;10: 225. pmid:31366061
- 78. López-Mercadal J, Delgado S, Mercadal P, Seguí G, Lalucat J, Busquets A, et al. Collection of data and information in Balearic Islands on biology of vectors and potential vectors of Xylella fastidiosa. EFSA Support Publ EN-6925. 2021;18: 1–136.
- 79. Karban R, Huntzinger M. Spatial and temporal refugia for an insect population declining due to climate change—ProQuest. 2021;12: 1–9.
- 80. Arbour G. A spittlebug in the lovage plant (Philaenus spumarius). In: Giles Arbour Bilingual Blog—Français/English [Internet]. 28 Jun 2009 [cited 18 Oct 2022]. https://gillesarbour.wordpress.com/2009/06/28/a-spittlebug-in-the-lovage-plant-philaenus-spumarius/
- 81. Palin MA. Ligusticum scoticum L. (Haloscias scoticum (L.)). J Ecol. 1988;76: 889–902.
- 82. Regnier R. Les Cicadelles écumantes de Normandie. Contribution à l’étude de Ptyelus graminis De Geer (Homoptere) et de ses variations. Bull Société Sci Nat Roue. 1936;70-71: 91–99.
- 83. Fabre J-H. La cicadelle écumeuse. Souvenirs Entomologiques (Septième Série), Études sur L’instinct et les Moeurs des Insectes. Paris: Libraire Delagrave; 1923. pp. 239–254.
- 84. Goetzke HH, Pattrick JG, Federle W. Froghoppers jump from smooth plant surfaces by piercing them with sharp spines. Proc Natl Acad Sci. 2019;116: 3012–3017. pmid:30718417
- 85. Georghiou GP. The insects and mites of Cyprus. With emphasis on species of economic importance to agriculture, forestry, man and domestic animals. Athens, Greece: Kiphissia; 1977.
- 86. Yurtsever S. Inheritance of three dorsal color/pattern morphs in some Turkish Philaenus spumarius (Homoptera: Cercopidae) populations. Isr J Zool. 1999;45: 361–369.
- 87. Wood ZM, Jones PL. The effects of host plant species and plant quality on growth and development in the meadow spittlebug (Philaenus spumarius) on Kent Island in the Bay of Fundy. Northeast Nat. 2020;27: 168–185.
- 88. Nickel B. Untersuchungen über die Ernährung und die Aussscheidungen einheimischer Cercopidenlarven. PhD thesis, Technische Universität, München. 1979.
- 89. Kiss B, Rédei D, Koczor S. Occurrence and feeding of hemipterans on common ragweed (Ambrosia artemisiifolia) in Hungary. Bull Insectology. 2008;61: 195–196.
- 90. Hoffman GD, McEvoy PB. Mechanical limitations on feeding by meadow spittlebugs Philaenus spumarius (Homoptera: Cercopidae) on wild and cultivated host plants. Ecol Entomol. 1985b;10: 415–426.
- 91. Fagan WF. Omnivory as a stabilizing feature of natural communities. Am Nat. 1997;150: 554–567. pmid:18811300
- 92. Villa M, Rodrigues I, Baptista P, Fereres A, Pereira JA. Populations and host/non-host plants of spittlebugs nymphs in olive orchards from northeastern Portugal. Insects. 2020;11: 720. pmid:33096613
- 93. Yurtsever S, Bakırcıoglu D, Karahalıl B. A preliminary study on the metal content of the spittle of two cercopoid insects (Hemiptera: Cercopoidea, Aphrophoridae). Entomol Mon Mag. 2012;148: 95–108.
- 94. Kambo DS. Differences in Performance and Herbivory Along a Latitudinal Gradient for Common Burdock (Arctium minus). MS thesis, University of Toronto. 2012. https://www.proquest.com/openview/3d724f30fec600cc04b26059562a7bff/1?pq-origsite=gscholar&cbl=18750
- 95. Rodríguez J, Cordero-Rivera A, González L. Impacts of the invasive plant Carpobrotus edulis on herbivore communities on the Iberian Peninsula. Biol Invasions. 2021;23: 1425–1441.
- 96. Rösch V, Schmitz G. Phytophagous arthropod fauna of Chinese Mugwort Artemisia verlotiorum, Lamotte, 1877 (Asteraceae) in Central Europe, particularly the Lake Constance region. Entomol Gen. 2014;35: 33–45.
- 97. Zeybekoğlu Ü, Turgut F. A study on the life cycle and population density of Philaenus spumarius (L.) (Hom: Cercopidae) in Samsun. Ondokuz Mayıs Üniversitesi Ziraat Fakültesi Derg Anadolu Tarım Bilim Derg. 2003;18: 49–54.
- 98. Sevarika M, Rondoni G, Ganassi S, Pistillo OM, Germinara GS, De Cristofaro A, et al. Behavioural and electrophysiological responses of Philaenus spumarius to odours from conspecifics. Sci Rep. 2022;12: 8402. pmid:35589785
- 99. Grant JF, Lambdin PL, Follum RA. Infestation levels and seasonal incidence of the meadow spittlebug (Homoptera: Cercopidae) on musk thistle in Tennessee. J Agric Entomol USA. 1998;15: 83–91.
- 100. Batra SWT, Coulson JR, Dunn PH, Boldt PE. Insects and Fungi Associated with Carduus Thistles (Compositae). U.S. Department of Agriculture, Technical Bulletin No. 1616. 1981.
- 101. Johnson JB, McCaffrey JP, Merickel FW. Endemic phytophagous insects associated with yellow starthistle in northern Idaho. Pan-Pac Entomol. 1992;68: 169–173.
- 102. Henderson G, Hoffman GD, Jeanne RL. Predation on cercopids and material use of the spittle in aphid-tent construction by prairie ants. Psyche (Stuttg). 1990;97: 43–53.
- 103. Batters J. The Impact of Invasive Thistle Species on Dynamics of Cercopidae in the Stikine-Skeena Region of Northern British Columbia. Undergraduate honors thesis, Lakehead University. 2020.
- 104. Lavigne R. Biology of Philaenus leucophthalmus (L.), In Massachusetts1. J Econ Entomol. 1959;52: 904–907.
- 105. Ochoa J. M J. Cultivo de cardo para la producción de biomasa. Surcos Aragón. 2000; 41–43.
- 106. Mesmin X, Chartois M, Borgomano S, Rasplus J-Y, Rossi J-P, Cruaud A. Interaction networks between spittlebugs and vegetation types in and around olive and clementine groves of Corsica; implications for the spread of Xylella fastidiosa. Agric Ecosyst Environ. 2022;334: 107979.
- 107. Weaver CR. Improvement in hay yields resulting from control of the meadow spittlebug. J Econ Entomol. 1950;43.
- 108. Karban R. Interspecific competition between folivorous insects on Erigeron glaucus. Ecology. 1986;67: 1063–1072.
- 109. Batra SWT. Insects associated with weeds of the northeastern United States: Quickweeds, Galinsoga ciliata and Galinsoga parviflora (Compositae). Enviromental Entomol. 1979;8: 1078–1082.
- 110. Cornara D, Sicard A, Zeilinger AR, Porcelli F, Purcell AH, Almeida RPP. Transmission of Xylella fastidiosa to grapevine by the meadow spittlebug. Phytopathology. 2016;106: 1285–1290. pmid:27392174
- 111. Randall J. Element stewardship abstract for Hemizonia pungens Torr. & Grey. The Nature Conservancy; undated. https://www.invasive.org/gist/esadocs/documnts/hemipun.rtf
- 112. Syrett P, Smith LA. The insect fauna of four weedy Hieracium (Asteraceae) species in New Zealand. N Z J Zool. 1998;25: 73–83.
- 113. Zeleny J, Havelka J, Slama K. Hormonally mediated insect-plant relationships: Arthropod populations associated with ecdysteroid-containing plant, Leuzea carthamoides (Asteraceae). Eur J Entomol. 1997;94: 183–198.
- 114. Hambäck PA. Direct and indirect effects of herbivory: Feeding by spittlebugs affects pollinator visitation rates and seedset of Rudbeckia hirta. Écoscience. 2001;8: 45–50.
- 115. Hardy J. Notes on cuckoo-flowers and the cuckoo spit. Edinb New Philos J. 1862;16 (New Series): 70–76.
- 116. Markheiser A, Cornara D, Fereres A, Maixner M. Analysis of vector behavior as a tool to predict Xylella fastidiosa patterns of spread. Entomol Gen. 2020;40: 1–13.
- 117. Jobin A, Schaffner U, Nentwig W. The structure of phytophagous insect fauna on the introduced weed Solidago altissima in Switzerland. Entomol Exp Appl. 1996;79: 33–42.
- 118. Wise MJ, Kieffer DL, Abrahamson WG. Costs and benefits of gregarious feeding in the meadow spittlebug, Philaenus spumarius. Ecol Entomol. 2006;31: 548–555.
- 119. Buchele DE, Baskin JM, Baskin CC. Ecology of the endangered species Solidago shortii. iii. Seed germination ecology. Bull Torrey Bot Club. 1991;118: 288–291.
- 120. Rodman GH. The story of the cuckoo spit. Proc Photomicrogr Soc. 1921;10: 31–42.
- 121. Ossiannilsson F. On the identity of Cicada spumaria Linneaus (1758) (Hemiptera. Homoptera), with notes on the breeding-plants of three Swedish cercopids. Opusc Entomol. 1950;15: 145–156.
- 122. Varty IW. A survey of the sucking insects of the birches in the maritime provinces. Can Entomol. 1963;95: 1097–1106.
- 123. Mazzoni V. Contribution to the knowledge of the Auchenorrhyncha (Hemiptera Fulgoromorpha and Cicadomorpha) of Tuscany (Italy). Redia. 2005;88: 85–102.
- 124. Wahlgren E. 1944. Cecidiologiska anteckningar. Entomol Tidskr. 65: 50–121.
- 125. Yates CN, Murphy SD. Observations of herbivore attack on garlic mustard (Alliaria petiolata) in Southwestern Ontario, Canada. Biol Invasions. 2008;10: 757–760.
- 126. Doering KC. Host plant records of Cercopidae in North America, North of Mexico (Homoptera). J Kans Entomol Soc. 1942;15: 65–72.
- 127. Zimmerman EC. Insects of Hawaii. Vol 4. Homoptera: Auchenorrhyncha. Honolulu: University of Hawaii Press; 1948.
- 128. McPartland JM, Clarke RC, Watson DP. Hemp Diseases and Pests: Management and Biological Control. CABI; 2000.
- 129. Waipara NW, Winks CJ, Smith LA, Wilkie JP. Natural enemies of Japanese honeysuckle Lonicera japonica in New Zealand. N Z Plant Prot. 2007;60: 158–163.
- 130. Batra SWT. Insects associated with weeds in the northeastern United States. iii. Chickweed, Stellaria media, and stitchwort, S. graminea (Caryophyllaceae). J N Y Entomol Soc. 1979;87: 223–235.
- 131. Nencioni A, Pastorelli R, Bigiotti G, Cucu MA, Sacchetti P. Diversity of the bacterial community associated with hindgut, Malpighian tubules, and foam of nymphs of two spittlebug species (Hemiptera: Aphrophoridae). Microorganisms. 2023;11: 466. pmid:36838431
- 132. Hamilton KGA, Morales CF. Cercopidae (Insecta: Homoptera). Fauna N Z. 1992;25.
- 133. Ward LK. The conservation of juniper: The associated fauna with special reference to southern England. J Appl Ecol. 1977;14: 81–120.
- 134. Halkka O, Raatikainen M, Halkka L, Raatikainen T. Coexistence of four species of spittle-producing Homoptera. Ann Zool Fenn. 1977;14: 228–231.
- 135. Frey-Gessner E. Beitrag zur Hemiptern-Fauna des Ober-Wallis. Mitteilungen Schweiz Entomol Ges. 1862;1: 24–31.
- 136. Hartley SE, Gardner SM. The response of Philaenus spumarius (Homoptera: Cercopidae) to fertilizing and shading its moorland host-plant (Calluna vulgaris). Ecol Entomol. 1995;20: 396–399.
- 137. Nixon D, Okely EF, Blackith RM. The distribution and morphometrics of spittle bugs on Irish blanket bog. Proc R Ir Acad B. 1975;75: 305–315. pmid:1161781
- 138. Silva L, Tavares J. Phytophagous insects associated with endemic, Macaronesian, and exotic plants in the Azores. Avances en entomología ibérica. Museo Nacional de Ciencias Naturales (CSIC) y Universidad Autónoma de Madrid; 1995. pp. 179–188. https://repositorio.uac.pt/handle/10400.3/789
- 139. Nunn ML, Hillier NK. Biodiversity and sweep sampling of selected leafhopper and beetle species in wild blueberries. J Acadian Entomol Soc. 2015;11: 17–21.
- 140. Maurice C, Bédard C, Fitzpatrick SM, Troubridge J, Henderson D. Integrated Pest Management for Cranberries in Western Canada, Technical Report #163. Agriculture and Agri-food Canada; 2000.
- 141. Whitfield GH, Ellis CR. The pest status of foliar insects on soybeans and white beans in Ontario. Proc Entomol Soc Ont. 1976;107: 47–55.
- 142. Mackun IR, Baker BS. Insect populations and feeding damage among birdsfoot trefoil–grass mixtures under different cutting schedules. J Econ Entomol. 1990;83: 260–267.
- 143. Ganassi S, Cascone P, Domenico CD, Pistillo M, Formisano G, Giorgini M, et al. Electrophysiological and behavioural response of Philaenus spumarius to essential oils and aromatic plants. Sci Rep. 2020;10: 3114. pmid:32080275
- 144. Germinara GS, Ganassi S, Pistillo MO, Di Domenico C, De Cristofaro A, Di Palma AM. Antennal olfactory responses of adult meadow spittlebug, Philaenus spumarius, to volatile organic compounds (VOCs). PloS One. 2017;12: e0190454. pmid:29287108
- 145. Macklin PR. Spittle insects as food of the red-winged blackbird. The Auk. 1958;75: 225–225.
- 146. Rekach VN, Dobretzova TA. A survey of insects injurious to utility and forage crops in Transcaucasia. 1935;45? x-42-y.
- 147. Everly RT. Evaluation of population estimates and rate of loss of forage for the meadow spittlebug, Philaenus leucophthalmus. Proc Indiana Acad Sci. 1958;68: 171–185.
- 148. Pearson WD. Effect of meadow spittlebug and Australian crop mirid on white clover seed production in small cages. N Z J Agric Res. 1991;34: 439–444.
- 149. Farnham NGJ. The polymorphism of Philaenus spumarius. Bull Amat Entomol Soc. 1983;42: 177–188.
- 150. Abdul-Nour H, Lahoud L. Révision du genre Philaenus Stål, 1864 au Liban, avec la description d’une nouvelle espèce P. arslani, n. sp. (Homoptera Auchenorrhyncha, Cercopoidea). Nouv Rev Entomol. 1995;12: 297–303.
- 151. Nixon P, McPherson J. An annotated list of phytophagous insects collected on immature black walnut trees in southern Illinois. Gt Lakes Entomol. 2017;10. Available: https://scholar.valpo.edu/tgle/vol10/iss4/8
- 152. Güçlü Ş, Hayat R, Özbek H. An investigation on phytophagous insect species on walnut (Juglans regia Linnaeus) in Erzurum and its neighbouring provinces. Turk J Entomol. 1995;19.
- 153. Reclaire A. Naamlijst der in Nederland en het aangrenzende gebied waargenomen Cicaden (Hemiptera-Homoptera). Entomol Ber. 11: 221–256.
- 154. Metin F, Zeybekoğlu Ü, Karaca İ. Insects on lavender in Isparta province, Turkey. Int J Agric Environ Food Sci. 2020;4: 425–431.
- 155. Neubauer S, Kral J, Klimes K. Insect pests of peppermint. Nase Liecive Rastl. 1974;11: 38–41.
- 156. Dunn AJ. Stachys germanica L. J Ecol. 1997;85: 531–539.
- 157. Jürisoo V. Agro-Ecological Studies on Leafhoppers (Auchenorrhyncha, Homoptera) and Bugs (Heteroptera) at Ekensgård Farm in the Province of Hälsingland, Sweden. PhD thesis, Stockholm University. 1964. http://urn.kb.se/resolve?urn=urn:nbn:se:su:diva-168741
- 158. Ellis D. Biological Control of Purple Loosestrife in Connecticut. Purdue University; 1997. http://www.ceris.purdue.edu/napis/states/ct/etpls/pls1997.html
- 159. Kaçar G, Başpınar H, Zeybekoğlu Ü, Ulusoy MR. Potential treat for olives: Philaenus spumarius (Linnaeus) (Cercopidae) and Auchenorrhyncha species (Hemiptera). 2017;57: 463–471.
- 160. MacGarvin M. Species-area relationships of insects on host plants: Herbivores on rosebay willowherb. J Anim Ecol. 1982;51: 207–223.
- 161. Puentes A, Johnson MTJ. Tolerance to deer herbivory and resistance to insect herbivores in the common evening primrose (Oenothera biennis). J Evol Biol. 2016;29: 86–97. pmid:26395768
- 162. Ivey CT, Carr DE. Effects of herbivory and inbreeding on the pollinators and mating system of Mimulus guttatus (Phrymaceae). Am J Bot. 2005;92: 1641–1649. pmid:21646081
- 163. Johnson WT, Lyon HH. Insects That Feed on Trees and Shrubs. Second Edition. Insects Feed Trees Shrubs. 1991; 560.
- 164. Speers CF. The pine spittle bug (Aphrophora parallela Say), Technical Publication No. 54. Bull N Y State Coll For. 1941;14: 1–65.
- 165. Yurtsever S. Records of spittle-producing insects (Hom., Cercopidae) in northwestern Turkey. Entomol Mon Mag. 2001;137: 77–78.
- 166. Biedermann R. Aggregationand survival of Neophilaenus albipennis (Hemiptera: Cercopidae) spittlebug nymphs. Eur J Entomol. 2003;100: 493–500.
- 167. Prestidge RA. Preliminary observations on the grassland leafhopper fauna of the central North Island Volcanic Plateau. N Z Entomol. 1989;12: 54–57.
- 168. Karahalıl B. Dorsal Colour/Pattern Phenotype Frequency of Philaenus spumarius (L.) in Some Turkish Populations and Host Plant Relations in Related Cercopidae Species. MS thesis, Trakya University. 2010.
- 169. Karadjova O, Krusteva H. Species composition and population dynamics of the harmful insect fauna (Hemiptera: Cicadomorpha, Fulgoromorpha and Sternorrhyncha) of winter triticale. Bulg J Agric Sci. 2017;22: 619–236.
- 170. Maneva V, Atanasova D, Nedelcheva T. Phytosanitary status and yield of kamut (Triticum turgidum polonicum L.) grown in organic and biodynamic farming. Agric Sci Technol. 2017;9: 42–44.
- 171. Garneau A. Liste de cicadaires récoltés en 1983 sur la rhubarb (Rheum rhaponticum L.) à Granby, Comté de Shefford. Fabreries. 1984;10: 77–79.
- 172. Beckett KIS, Robertson AB, Matthews PGD. Studies on gas exchange in the meadow spittlebug, Philaenus spumarius: the metabolic cost of feeding on, and living in, xylem sap. J Exp Biol. 2019;222: jeb191973. pmid:30745324
- 173. Kwon O. Population dynamics of insects associated with Rumex obtusifolius in different habitats. Entomol Res. 2006;36: 73–78.
- 174. Winterbourn MJ. The arthropod fauna of bracken (Pteridium aquilinum) on the Port Hills, South Island, New Zealand. N Z Entomol. 1987;10: 99–104.
- 175. Lawton JH. The structure of the arthropod community on bracken. Bot J Linn Soc. 1976;73: 187–216.
- 176. Halarewicz A. Fulgoromorpha and Cicadomorpha (Hemiptera) infesting bracken (Pteridium aquilinum). Pol J Entomol. 2011;80: 451–456.
- 177. Yoder MV, Skinner LC, Ragsdale DW. Common buckthorn, Rhamnus cathartica L.: Available feeding niches and the importance of controlling this invasive woody perennial in North America. Proceedings of the XII International Symposium on Biological Control of Weeds, La Grande Motte, France, 22–27 April, 2007. CABI; 2008. pp. 232–237.
- 178. Osborn H. Meadow and Pasture Insects. Columbus, Ohio: The Educators’ Press; 1939.
- 179. Pollard E. Hedges. ii. The effect of removal of the bottom flora of a hawthorn hedgerow on the fauna of the hawthorn. J Appl Ecol. 1968;5: 109–123.
- 180. Cole DH, Ashman T-L. Sexes show differential tolerance to spittlebug damage and consequences of damage for multi-species interactions. Am J Bot. 2005;92: 1708–1713. pmid:21646088
- 181. Crews LJ, McCully ME, Canny MJ, Huang CX, Ling LEC. Xylem feeding by spittlebug nymphs: some observations by optical and cryo-scanning electron microscopy. Am J Bot. 1998;85: 449–460. pmid:21684926
- 182. Jenser G, Hegab AM. On the distribution of Philaenus spumarius (Linné) imagoes on fruit-trees and the undergrowth (Homoptera). Folia Entomol Hung. 32: 231–233.
- 183. Cleaveland ML, Hamilton DW. The insect fauna of apple trees in southern Indiana, 1956 and 1957. Proc Indiana Acad Sci. 1958;68: 205–217.
- 184. Bleicher K, Orosz A, Cross J, Markó V. Survey of leafhoppers, planthoppers and froghoppers (Auchenorrhyncha) in apple orchards in South-East England. Acta Phytopathol Entomol Hung. 2010;45: 93–105.
- 185. Batra SWT. Insects associated with weeds in the northeastern United States. ii. Cinquefoils, Potentilla norvegica and P. recta (Rosaceae). J N Y Entomol Soc. 1979;87: 216–222.
- 186. Anonymous. Spectacular concentration. Can Insect Pest Rev. 1945;23: 218–219.
- 187. Phillips JHH. An annotated list of Hemiptera inhabiting sour cherry orchards in the Niagara Peninsula, Ontario. Can Entomol. 1951;83: 194–205.
- 188. Hasbroucq S, Casarin N, Czwienczek E, Bragard C, Grégoire J-C. Distribution, adult phenology and life history traits of potential insect vectors of Xylella fastidiosa in Belgium. Belg J Entomol. 2020;92: 1.
- 189. Osborn H. Homoptera in the Vicinity of Cranberry Lake. Papers from the Department of Forest Entomology, Technical Publication No 16. New York State College of Forestry at Syracuse University; 1922. pp. 24–54.
- 190. Angelova R, Gjonov I. Spittlebugs (Hemiptera: Cercopoidea) of Sarnena Sredna Gora (Bulgaria). ZooNotes. 2022.
- 191. Massee AM. The Hemiptera–Homoptera (Auchenorhyncha) associated with cultivated fruits. J Soceity Br Entomol. 1941;2: 99–109.
- 192. Batra SWT. Phytophages and Pollinators of Galium (Rubiaceae) in Eurasia and North America. Environ Entomol. 1984;13: 1113–1124.
- 193. Schnaider Z. Feeding of Aphrophora spp. in osier beds, and control trials. Sylwan. 1960;104: 41–5.
- 194. Owen DF, Whiteway WR. Buddleia davidii in Britain: History and development of an associated fauna. Biol Conserv. 1980;17: 149–155.
- 195. Lambillion L-J. La cicadelle ecumeuse (Aphrophora spumaria Linne). Rev Mens Soc Entomol Namuroise. 1914; 71–73.
- 196. Patch EM. Aroostook potato insects. J Econ Entomol. 1922;15: 372–373.
- 197. Girsova NV, Bottner-Parker KD, Bogoutdinov DZ, Meshkov YI, Mozhaeva KA, Kastalyeva TB, et al. Diverse phytoplasmas associated with potato stolbur and other related potato diseases in Russia. Eur J Plant Pathol. 2016;145: 139–153.
- 198. Carle P, Moutous , Gilberte . Observations sur le mode de nutrition sur vigne de quatre espèces de cicadelles. Ann Epiphyt. 1965;16: 333–354.
- 199. Krstić O, Radonjić S, Hrnčić S, Cvrković T, Mitrović M, Kosovac A, et al. Diversity of the Auchenorrhyncha fauna in vineyards of Montenegro. Zašt Bilja. 2012;63: 108–113.
- 200. Rodrigues I, Rebelo MT, Baptista P, Pereira JA. Cicadomorpha community (Hemiptera: Auchenorrhyncha) in Portuguese vineyards with notes of potential vectors of Xylella fastidiosa. Insects. 2023;14: 251. pmid:36975936
- 201. Warren LO, Tadic M. The Fall Webworm, Hyphantria cunea (Drury). Bulletin 759. University of Arkansas, Agricultural Experiment Station, Fayetteville; 1970.
- 202. Brockerhoff EG, Suckling DM, Ecroyd CE, Wagstaff SJ, Raabe MC, Dowell RV, et al. Worldwide host plants of the highly polyphagous, invasive Epiphyas postvittana (Lepidoptera: Tortricidae). J Econ Entomol. 2011;104: 1514–1524. pmid:22066180
- 203. Young OP. Host plants of the tarnished plant bug, Lygus lineolaris (Heteroptera: Miridae). Ann Entomol Soc Am. 1986;79: 747–762.
- 204. Loxdale HD, Balog A, Harvey JA. Generalism in nature…the great misnomer: Aphids and wasp parasitoids as examples. Insects. 2019;10: 314. pmid:31554276
- 205. Pearce SL, Clarke DF, East PD, Elfekih S, Gordon KHJ, Jermiin LS, et al. Genomic innovations, transcriptional plasticity and gene loss underlying the evolution and divergence of two highly polyphagous and invasive Helicoverpa pest species. BMC Biol. 2017;15: 63. pmid:28756777
- 206. Leonard DE. Bioecology of the gypsy moth. The Gypsy Moth: Research Toward Integrated Pest Management Forest Service Technical Bulletin 1584. Washington, D. C.: U. S. U.S. Department of Agriculture; 1981. pp. 9–29.
- 207. Ballesteros Mejia L, Arnal P, Hallwachs W, Haxaire J, Janzen D, Kitching IJ, et al. A global food plant dataset for wild silkmoths and hawkmoths and its use in documenting polyphagy of their caterpillars (Lepidoptera: Bombycoidea: Saturniidae, Sphingidae). Biodivers Data J. 2020;8: e60027. pmid:33343218
- 208. Barringer L, Ciafré C. Worldwide feeding host plants of spotted lanternfly, with significant additions from North America. Environ Entomol. 2020;49. pmid:32797186
- 209. Normark BB, Johnson NA. Niche explosion. Genetica. 2011;139: 551–564. pmid:21104426
- 210. Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, et al. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature. 2011;479: 487–492. pmid:22113690
- 211. Ossiannilsson F. The Auchenorrhyncha (Homoptera) of Fennoscandia and Denmark. Part 2: the families Cicadidae, Cercopidae, Membracidae, and Cicadellidae (excl. Deltocephalinae). Fauna Entomol Scand. 1981;7: 223–593.
- 212. Chartois M, Mesmin X, Quiquerez I, Borgomano S, Farigoule P, Pierre É, et al. Environmental factors driving the abundance of Philaenus spumarius in mesomediterranean habitats of Corsica (France). Sci Rep. 2023;13: 1901. pmid:36732346
- 213. Halkka O, Mikkola E. The selection regime of Philaenus spumarius (L.) (Homoptera). In: Christiansen FB, Fenchel TM, editors. Measuring Selection in Natural Populations. Berlin, Heidelberg: Springer; 1977. pp. 445–463.
- 214. Thompson V. Spittlebug indicators of nitrogen-fixing plants. Ecol Entomol. 1994;19: 391–398.
- 215. Hamilton KGA. The Spittlebugs of Canada. Homoptera: Cercopidae. The Insects and Arachnids of Canada. Part 10. Publication 1740. Ottawa: Agriculture Canada; 1982.
- 216. Thorne M, Wilson S, Wright M, Peck D. Twolined Spittlebug Identification Key. College of Tropical Agriculture and Human Resources, University of Hawai‘i at Manoa; 2022.
- 217. Ashcroft T, George S. New to New Zealand: Bathyllus albicinctus (Hemiptera: Aphrophoridae) Whangarei. Initial Investigation & Technical Report/Entomology. 7 pp. New Zealand Ministry of Agriculture and Forestry; 2004.
- 218. Rösch V, Marques E, Miralles-Núñez A, Zahniser JN, Wilson MR. Draeculacephala robinsoni Hamilton, 1967 (Hemiptera: Auchenorrhyncha: Cicadellidae), a newly introduced species and genus in Europe with comments on its identification. Zootaxa. 2022;5116: 439–448. pmid:35391325
- 219. Sergel R. Area expansion of the imported Nearctic cicadelline leafhopper Graphocephala fennahi Young, 1977 in Western Europe (Homoptera: Auchenorrhyncha). Articulata. 1987;3: 21–22.
- 220. Hill KBR, Marshall DC, Cooley JR. Crossing Cook Strait: Possible human transportation and establishment of two New Zealand cicadas from North Island to South Island (Kikihia scutellaris and K. ochrina, Hemiptera: Cicadidae). N Z Entomol. 2005;28: 71–80.
- 221. Maryańska-Nadachowska A, Kuznetsova VG, Lachowska D, Drosopoulos S. Mediterranean species of the spittlebug genus Philaenus: Modes of chromosome evolution. J Insect Sci. 2012;12.
- 222. Drosopoulos S, Maryańska-Nadachowska A, Kuznetsova VG. The Mediterranean: Area of origin of polymorphism and speciation in the spittlebug Philaenus (Hemiptera, Aphrophoridae). Zoosystematics Evol. 2010;86: 125–128.
- 223. Boukhris-Bouhachem S, Souissi R, Abou Kubaa R, El Moujabber M, Gnezdilov V. Aphrophoridae as potential vectors of Xylella fastidiosa in Tunisia. Insects. 2023;14: 119. pmid:36835688
- 224. Drosopoulos S, Quartau JA. The spittle bug Philaenus tesselatus Melichar, 1899 (Hemiptera, Auchenorrhyncha, Cercopidae) is a distinct species. Zootaxa. 2002;68: 1–8.
- 225. Maryańska-Nadachowska A, Drosopoulos S, Lachowska D, Kajtoch Ł, Kuznetsova VG. Molecular phylogeny of the Mediterranean species of Philaenus (Hemiptera: Auchenorrhyncha: Aphrophoridae) using mitochondrial and nuclear DNA sequences. Syst Entomol. 2010;35: 318–328.
- 226. Loxdale HD, Harvey JA. The ‘generalism’ debate: misinterpreting the term in the empirical literature focusing on dietary breadth in insects. Biol J Linn Soc. 2016;119: 265–282.
- 227. Biello R, Mathers TC, Mugford ST, Liu Q, Rodrigues ASB, Neto AC, et al. Draft genome assembly version 1 of the meadow spittlebug Philaenus spumarius (Linnaeus, 1758) (Hemiptera, Aphrophoridae). Zenodo; 2020.
- 228. Thompson V. Insect-plant-fungus interactions in mycorrhizal associations, with a focus on spittlebugs and ectomycorrhizal host plants. Ecol Entomol. 2022;47: 915–929.
- 229. Singer MS. Evolutionary ecology of polyphagy. Tilmon K., (ed.). Specialization, Speciation, and Radiation–Evolutionary Biology of Herbivorous Insects. Berkeley: University of California Press; 2008. pp. 29–42.
- 230. Jaenike J. Host specialization in phytophagous insects. Annu Rev Ecol Syst. 1990;21: 243–273.
- 231. Forister ML, Novotny V, Panorska AK, Baje L, Basset Y, Butterill PT, et al. The global distribution of diet breadth in insect herbivores. Proc Natl Acad Sci. 2015;112: 442–447. pmid:25548168
- 232. Formisano G, Iodice L, Cascone P, Sacco A, Quarto R, Cavalieri V, et al. Wolbachia infection and genetic diversity of Italian populations of Philaenus spumarius, the main vector of Xylella fastidiosa in Europe. PLOS ONE. 2022;17: e0272028. pmid:36037217
- 233. Maryańska-Nadachowskaa A, Sanaieb E, Kajtocha Ł. High genetic diversity in southwest Asian populations of Philaenus spumarius (Hemiptera: Auchenorrhyncha). Zool Middle East. 2015;61: 264–272.
- 234. Lester K, Murphy K, McCluskey A, Cairns R, Fraser K, Kenyon D. Xylella fastidiosa: an overview of research at SASA. The Dundee Conference, Crop Production in Northern Britain, Dundee, UK, 25–26 February 2020. The Association for Crop Protection in Northern Britain; 2020. pp. 45–50.
- 235. Hoffman GD, McEvoy PB. The mechanism of trichome resistance in Anaphalis margaritacea to the meadow spittlebug Philaenus spumarius. Entomol Exp Appl. 1985a;39: 123–129.
- 236. Wheeler AG. Phytophagous arthropod fauna of crownvetch in Pennsylvania. Can Entomol. 1974;106: 897–908.
- 237. Morente M, Ramírez M, Lago C, de las Heras-Bravo D, Benito A, Moreno A, et al. Habitat manipulation for sustainable management of Philaenus spumarius, the main vector of Xylella fastidiosa in Europe. Pest Manag Sci. 2022;78: 4183–4194.
- 238. Wheeler AG. Lepyronia coleoptrata (Homoptera: Cercopidae), an immigrant spittlebug in North America: Distribution, seasonal history, and host plants. Proc Entomol Soc Wash. 1991;93: 463–470.
- 239. Press MC, Whittaker JB. Exploitation of the xylem stream by parasitic organisms. Philos Trans R Soc Lond B Biol Sci. 1993;341: 101–111.
- 240. Purcell AH, Finlay A. Evidence for noncirculative transmission of Pierce’s Disease bacterium by sharpshooter leafhoppers. Phytopathology. 1979;69: 393–395.
- 241. Avosani S, Nieri R, Mazzoni V, Anfora G, Hamouche Z, Zippari C, et al. Intruding into a conversation: How behavioral manipulation could support management of Xylella fastidiosa and its insect vectors. J Pest Sci. 2023 [cited 27 May 2023].
- 242. Avosani S, Daher E, Franceschi P, Ciolli M, Verrastro V, Mazzoni V. Vibrational communication and mating behavior of the meadow spittlebug Philaenus spumarius. Entomol Gen. 2020;40: 351–363.
- 243. Cruaud A, Gonzalez A-A, Godefroid M, Nidelet S, Streito J-C, Thuillier J-M, et al. Using insects to detect, monitor and predict the distribution of Xylella fastidiosa: a case study in Corsica. Sci Rep. 2018;8: 15628. pmid:30353142
- 244. Pocock MJO, Tweddle JC, Savage J, Robinson LD, Roy HE. The diversity and evolution of ecological and environmental citizen science. PLOS ONE. 2017;12: e0172579. pmid:28369087
- 245. Miller-Rushing A, Primack R, Bonney R. The history of public participation in ecological research. Front Ecol Environ. 2012;10: 285–290.
- 246. Lewandowski E, Specht H. Influence of volunteer and project characteristics on data quality of biological surveys. Conserv Biol. 2015;29: 713–723. pmid:25800171
- 247. Poisson AC, McCullough IM, Cheruvelil KS, Elliott KC, Latimore JA, Soranno PA. Quantifying the contribution of citizen science to broad-scale ecological databases. Front Ecol Environ. 2020;18: 19–26.
- 248. Sumner S, Bevan P, Hart AG, Isaac NJB. Mapping species distributions in 2 weeks using citizen science. Insect Conserv Divers. 2019;12: 382–388.