Prokelisia marginata -

Prokelisia marginata occurs along the American east coast from Massachusetts to Louisiana. This planthopper is very abundant in this area, and it is the primary grazer of the Smooth cordgrass Spartina alterniflora ^[2-4].

Prokelisia marginata got reported in isolated intertidal areas in California, on the Pacific coast ^[4]. Here, it occurs on another cordgrass species, namely Spartina foliosa ^[2]. There are indications that the pacific populations were introduced recently (after the 1970s) from the American east coast ^{[5, 6]}

 

First observation in Belgium

The Belgian cordgrass population was investigated, after Prokelisia marginata was found on the 20th of August 2011 in the Netherlands on the Common cordgrass Spartina townsendii var. anglica. As a result of this study, several hundred individuals were collected in the Bay of Heist on the 26th of August 2011 ^[7].

In 2010, this planthopper was already present in our southern and northern neighbouring countries. Therefore, it is assumed that its introduction took place in 2010 ^[7].

 

Spreading in Belgium

In Belgium, Prokelisia marginata is present on Common cordgrass in the Bay of Heist and the Zwin Nature Park in Knokke ^[7]. At other locations where its host plant occurs (e.g. in Nieuwpoort and along the Sea Scheldt), Prokelisia marginata has not yet been observed.

In the study area, Prokelisia marginata also occurs on Common cordgrass that grows along the Western Scheldt in Hoofdplaat, between Breskens and Terneuzen ^[7].

 

Spreading in neighbouring countries

In 1994, Prokelisia marginata was found in Europe for the first time, more specifically in the Algarve (Portugal). Later the species was reported in Spain (1998) and Slovenia (Adriatic Sea) (2004) ^[8].

In 2008, Prokelisia marginata was present in England, along the coast of the country of Hampshire (Portsmouth) ^[9]. The species arrived in France in 2009 ^[8]. In 2009, this species was common on cordgrass growing along the coast of the English county of Kent (Dover), although it was not found there yet in 2007. This indicates that the species spread rapidly across the English south coast ^[9].

In 2010, this species got sighted in the Netherlands, where it thrives, among other places, along the Eastern Scheldt ^[7].

 

Because cordgrass is sometimes used as a packaging material for oysters, the transport of oysters played a role in the introduction of Prokelisia marginata from America to Europe ^{[7, 9]}. The eggs of this species could have been present between the cordgrass leaves ^[7].

After its introduction to France, the species quickly expanded its range naturally. The introductions to Spain, France and Slovenia might have occurred independently ^[7]

 

Common cordgrass, a suitable hostplant for Prokelisia marginata, occurs in the intertidal area of the Belgian coast (Nieuwpoort, Bay of Heist, the Zwin Nature Park and the Scheldt Estuary) [10]. Common cordgrass is a non-native species, created in the 19th century along the south English coast after hybridization between the native Small cordgrass Spartina maritima and non-native Smooth cordgrass Spartina alterniflora [11].

Prokelisia marginata can only flourish on species of cordgrass ^[6]. Its distribution is linked to that of this plant, which typically occurs in intertidal areas on mudflats and salt marshes ^[10].

After its introduction, Prokelisia marginata can reach high densities of over 50,000 individuals per m² ^[5]. Besides the short-winged (brachypterous) individuals, there is also a long-winged (macropterous) kind. The latter is better at flying ^[3]. Once in the air, these small insects are transported by the wind. So, there is no directional dispersal. In many Swedish populations, there is a high number of long-winged individuals. These ensure the quick establishment of new populations at considerable distances from the already established ones. Large source populations cause a ‘rain’ of Prokelisia marginata along the Belgian coast ^[12].

Short-winged individuals have the advantage of being able to reproduce at a younger age ^[3]. The ratio of short-winged to long-winged individuals in a population is determined by several environmental factors, such as the quality of the host plant and the population density ^{[3, 13]}. High-density populations produce more long-winged individuals than populations with a low density.

Cold temperature is possibly the limiting factor for the northern distribution of this species. The species survives during the winter as nymphs (the life stage in which the planthopper already resembles the adult individuals, or ‘imago’, but wings are still lacking) between dead material ^[4], coiled leaves of old stems and in the leaf axis of young plants ^[6]. A decrease in population density can occur as a consequence of a long cold period prior to spring ^{[9, 14]}. Harsh winters can decrease densities so severely that the population is unable to recover during the following summer. Because of this, the northern boundary of this species along the American east coast is in Massachusetts ^{[5, 7]}.

In the United States, storms play an important role in the spread of this planthopper. Cordgrass populations along creeks and in lower areas are destroyed by winter storms and the loose plant material, in which Prokelisia marginata nymphs spend the winter, is washed away. At such places, Prokelisia marginata needs to reestablish itself each year.

During high tide, the adult survives submerged by creating air bubbles underneath its wings and by holding on to the inside of a folded leaf. The species can also remain on the water surface and jump ^{[14, 15]}.

Prokelisia marginata occurs on Smooth cordgrass (Spartina alterniflora), Small cordgrass (S. maritima) and Common cordgrass (S. anglica). This species easily adapts to new Spartina species ^[14]

 

Both the imago and nymph feed exclusively on the nutrient-rich sap (phloem) of cordgrass. Females lay their eggs with an ovipositor in the vascular tissue, the canal system through which the plant transports water and phloem. Because of this, the plants get brown spots and produce less viable seeds ^{[6, 7]}.

Common cordgrass that grows along the east coast of the United States, the original distribution area of P. marginata, appeared less affected by this insect's presence compared to cordgrass in regions where P. marginata previously did not occur. An experiment in a greenhouse has shown that Smooth cordgrass can be severely damaged by high predation of Prokelisia marginata ^[16]. Other experiments show that the planthopper can reach up to 200 individuals per plant within two generations after its introduction. This corresponds with over 50,000 cicadas per m² ^[16]. Such numbers can lead to the death of cordgrass ^[6].

The difference in sensitivity of cordgrass to Prokelisia marginata probably has a genetic basis. Cordgrass populations in regions where this insect does not traditionally occur are less resistant ^{[17, 18]}. On resistant cordgrass populations, Prokelisia marginata reaches abundances that are 10 times lower than with less resistant populations and its presence usually doesn’t lead to the host’ death ^[18].

This planthopper is an interesting organism for biological control of non-native cordgrass due to the species-specific negative influence it can have on cordgrass. In 2000, this insect was successfully introduced to Common cordgrass, invasive in Willapa Bay and Puget Sound (Washington State, United States) ^{[5, 6]}. It was feared that the cordgrass would eventually become resistant to this planthopper ^{[17, 18]}. In 2007, the entire region got sprayed with herbicides to eradicate the invasive cordgrass. This measure creates uncertainty about the effectiveness of Prokelisia marginata as a biological control agent ^[5].

The future will show if Common cordgrass, an invasive species with a negative influence on native soil species and coastal birds ^{[19, 20]}, will be affected by the arrival of this planthopper in our regions.

The population density of this planthopper can be influenced by the presence of two parasites, namely Pseudogonatopus arizonicus (family Dryinidae) and Elenchus koebelei (order Strepsiptera) ^[21]

 

Prokelisia marginata is a typical Delphacidae: a relatively small insect (2.3 to 4.4 mm ^[2]) that feeds on the phloem of cordgrasses ^[6]. This species has a yellow to light brown head and body which horizontal brown stripes ^[2]. P. marginata reproduces sexually. Males actively seek females, and the two sexes communicate through acoustic signals, transmitted as vibrations through the host plant ^[22]. These signals are species-specific and help maintain reproductive isolation between sympatric Prokelisia species ^[23].

Prokelisia marginata can be distinguished from the other Delphacidae that occur in the Benelux with the aid of reference work ^[24].

The size of adults is positively correlated with their fertility. The higher the brood temperature, the faster the larvae grow. However, this reduces their survival chance ^[25].

Like most planthoppers, this species shows wing dimorphism (Figure 1). In a single population, there are two types of individuals: long- and short-winged planthoppers ^[26]. Long-winged individuals can fly and disperse much further (up to 30 km) than individuals without wings. Whether or not a planthopper grows wings during its development depends on the population density and the nutrient content of the host plant. Winged individuals occur more often in unstable habitats, while non-winged planthoppers, which have greater fertility, occur in stable environments with low densities ^[27].

Although planthoppers are not well known to the general public, they are responsible for the familiar phenomenon called ‘cuckoo spit’ (in Dutch: ‘koekoeksspuug’). This is the foam-like substance often found on plants, produced and whipped up by the nymphs of spittlebugs (a different family of planthoppers than Delphacidae, to which Prokelisia marginata belongs). The body of the nymph is completely surrounded by the foam, which protects against dehydration, parasites and predators. These nests are called ‘cuckoo spit’ because people used to think they came from a cuckoo spitting on the plant. The ragged robin’s Dutch name (‘Echte koekoeksbloem’) owes its name to the ‘cuckoo spit’ that is often present on the stem of this flower ^[28].

Figure 1: At the top – a macropterous (long-winged) individual. At the bottom – a brachypterous (short-winged) individual. Not only is the last pair of wings of a short-winged individual strongly reduced, but the first pair of wings is also less developed ^[3].

[1]          World Register of Marine Species (WoRMS) (2020). Prokelisia marginata (Van Duzee, 1897). [http://www.marinespecies.org/aphia.php?p=taxdetails&id=503319] (2020-11-17).

[2]          Wilson, S.W. (1982). The planthopper genus Prokelisia in the United States (Homoptera: Fulgoroidea: Delphacidae). J. Kans. Entomol. Soc. 55(3): 532-546. [http://www.vliz.be/imis/imis.php?module=ref&refid=213611]

[3]          Denno, R.F.; Douglas, L.W.; Jacobs, D. (1985). Crowding and host plant nutrition: Environmental determinants of wing-form in Prokelisia marginata. Ecology 66(5): 1588-1596. [http://www.vliz.be/imis/imis.php?module=ref&refid=213596]

[4]          Denno, R.F.; Schauff, M.E.; Wilson, S.W.; Olmstead, K.L. (1987). Practical diagnosis and natural history of two sibling salt marsh-inhabiting planthoppers in the genus Prokelisia (Homoptera, Delphacidae). Proc. Entomol. Soc. Wash. 89(4): 687-700. [http://www.vliz.be/en/imis?module=ref&refid=213597]

[5]          Grevstad, F.S.; Switzer, R.W.; Wecker, M.S. (2003). Habitat trade-offs in the summer and winter performance of the planthopper Prokelisia marginata introduced against the intertidal grass Spartina alterniflora in Willapa Bay, Washington, in: Cullen, J.M. et al. Proceedings of the XI International Symposium on Biological Control of Weeds Canberra, Australia, 27 April-2 May 2003. CSIRO Entomology: Canberra: pp. 523-528. [http://www.vliz.be/imis/imis.php?module=ref&refid=213602]

[6]          Grevstad, F.S.; Strong, D.R.; Garcia-Rossi, D.; Switzer, R.W.; Wecker, M.S. (2003). Biological control of Spartina alterniflora in Willapa Bay, Washington using the planthopper Prokelisia marginata: agent specificity and early results. Biol. Control. 27(1): 32-42. [http://www.vliz.be/imis/imis.php?module=ref&refid=213180]

[7]          De Blauwe, H. (2011). De Slijkgrascicade Prokelisia marginata (Hemiptera: Delphacidae), een exoot gebonden aan Engels slijkgras Spartina townsendii, verovert nu ook de Belgische kust. De Strandvlo 31(3-4): 80-88. [http://www.vliz.be/imis/imis.php?module=ref&refid=211692]

[8]          Mifsud, D.; Cocquempot, C.; Mühlethaler, R.; Wilson, M.; Streito, J.-C. (2010). Other Hemiptera Sternorrhyncha (Aleyrodidae, Phylloxeroidea, and Psylloidea) and Hemiptera Auchenorrhyncha, in: Roques, A. et al. Alien terrestrial arthropods of Europe., 4. Pensoft Publishers: Sofia: pp. 511-552. [http://www.vliz.be/imis/imis.php?module=ref&refid=213606]

[9]          Badmin, J.; Witts, T. (2009). Cord-grass planthopper Prokelisia marginata (Hemiptera: Delphacidae) sweeps into Kent. Br. J. Entomol. Nat. Hist. 22(4): 213-215. [http://www.vliz.be/imis/imis.php?module=ref&refid=213064]

[10]        Van Landuyt, W.; Hoste, I.; Vanhecke, L.; Van Den Bremt, P.; Vercruysse, W.; de Beer, D. (Ed.) (2006). Atlas van de flora van Vlaanderen en het Brussels Gewest. Nationale Plantentuin van België/Instituut voor Natuur- en Bosonderzoek/Flo.Wer: Brussel. ISBN 90-726-1968-4. 1007 pp. [http://www.vliz.be/nl/catalogus?module=ref&refid=170947]

[11]        Ayres, D.R.; Strong, D.R. (2001). Origin and genetic diversity of Spartina anglica (Poaceae) using nuclear DNA markers. Am. J. Bot. 88(10): 1863-1867. [http://www.vliz.be/imis/imis.php?module=ref&refid=207303]

[12]        den Bieman, K. (2012). Persoonlijke mededeling

[13]        Strong Jr., D.R.; Stiling, P.D. (1983). Wing dimorphism changed by experimental density manipulation in a planthopper (Prokelisia marginata, Homoptera, Delphacidae). Ecology 64(1): 206-209. [http://www.vliz.be/imis/imis.php?module=ref&refid=214089]

[14]        Ouvrard, D.; Soulier-Perkins, A. (2012). Prokelisia marginata (Van Duzee, 1897) lands on the French coast of Normandy (Hemiptera, Fulgoromorpha, Delphacidae). Bull. Soc. Entomol. Fr. 117(4): 441-444. [http://www.vliz.be/nl/catalogus?module=ref&refid=297715]

[15]        Arndt, C.H. (1914). Some insects of the between tides zone. Proc. Indiana Acad. Sci. 1182: 323-336. [http://www.vliz.be/nl/catalogus?module=ref&refid=302010]

[16]        Wu, M.-Y.; Hacker, S.D.; Ayres, D.R.; Strong, D.R. (1999). Potential of Prokelisia spp. as biological control agents of English cordgrass, Spartina anglica. Biol. Control. 16(3): 267-273. [http://www.vliz.be/imis/imis.php?module=ref&refid=213062]

[17]        Garcia-Rossi, D.; Rank, N.; Strong, D.R. (2003). Potential for self-defeating biological control? Variation in herbivore vulnerability among invasive Spartina genotypes. Ecol. Appl. 13(6): 1640-1649. [http://www.vliz.be/imis/imis.php?module=ref&refid=213607]

[18]        Strong, D.R. (2003). Evolving weeds and biological control, in: Cullen, J.M. et al. Proceedings of the XI International Symposium on Biological Control of Weeds Canberra, Australia, 27 April-2 May 2003. CSIRO Entomology: Canberra: pp. 21-27. [http://www.vliz.be/imis/imis.php?module=ref&refid=213610]

[19]        Nehring, S.; Adersen, H. (2006). NOBANIS - Invasive Alien Species Fact Sheet - Spartina anglica. NOBANIS - North European and Baltic Network on Invasive Alien Species: Copenhagen. 13 pp. [http://www.vliz.be/imis/imis.php?module=ref&refid=207302]

[20]        Minchin, D. (2009). Spartina anglica Hubbard, Common cordgrass (Poaceae, Magnoliophyta), in: DAISIE (Delivering Alien Invasive Species Inventories for Europe). Handbook of alien species in Europe. Invading Nature - Springer Series in Invasion Ecology, 3. Springer: Dordrecht: pp. 297. [http://www.vliz.be/imis/imis.php?module=ref&refid=135057]

[21]        Stiling, P.D.; Throckmorton, A.; Silvanima, J.; Strong, D.R. (1991). Biology of and rates of parasitism by nymphal and adult parasites of the salt-marsh inhabiting planthoppers Prokelisia marginata and P. dolus. Fla. Entomol. 74(1): 81-87. [http://www.vliz.be/nl/catalogus?module=ref&refid=297618]

[22]        Harkin, C. (2016). Ecological interactions of an invading insect: the planthopper Prokelisia marginata. PhD Thesis. University of Sussex: Sussex. xiv, 193 pp. [http://www.vliz.be/nl/catalogus?module=ref&refid=301875]

[23]        Heady, S.E.; Denno, R.F. (1991). Reproductive isolation in Prokelisia planthoppers (Homoptera, Delphacidae) - Acoustic differentiation and hybridization failure. J. Insect Behav. 4(3): 367-390. [http://www.vliz.be/nl/catalogus?module=ref&refid=301876]

[24]        den Bieman, K.; Biedermann, R.; Nickel, H.; Niedringhaus, R. (2011). The planthoppers and leafhoppers of Benelux, Identification keys to all families and genera and all Benelux species not recorded from Germany. Cicadina: Fachorgan des Arbeitskreises Zikaden Mitteleuropas., 2011. Wissenschaftlich Akademischer Buchvertrieb–Fründ: Scheessel. ISBN 978-3-939202-03-5.  pp. [http://www.vliz.be/en/imis?module=ref&refid=214183]

[25]        Denno, R.F.; Perfect, J.R. (Ed.) (1994). Planthoppers: their ecology and management. Springer US. ISBN 978-0-412-02341-5. 799 pp. [http://www.vliz.be/nl/catalogus?module=ref&refid=297718]

[26]        Denno, R.F.; Douglass, L.W.; Jacobs, D. (1986). Effects of Crowding and Host Plant Nutrition on a Wing-Dimorphic Planthopper. Ecology 67(1): 116-123. [http://www.vliz.be/nl/catalogus?module=ref&refid=302008]

[27]        Denno, R.F.; Grissell, E.E. (1979). The adaptiveness of wing-dimorphism in the salt marsh-inhabiting planthopper, Prokelisia marginata (Homoptera, Delphacidae). Ecology 60(1): 221-236. [http://www.vliz.be/en/imis?module=ref&refid=214146]

[28]        Wikipedia, de vrije encyclopedie (2018). Cicaden. [https://nl.wikipedia.org/wiki/Cicaden] (2012-03-09).

VLIZ Alien Species Consortium (2020). Prokelisia marginata. Non-native species of the Belgian part of the North Sea and bordering estuaries anno 2020. Flemish Institute for the Sea (VLIZ). 8 pp.