Cixiidae (Hemiptera: Fulgoromorpha)

The Cixiidae Spinola 1839 are a cosmopolitan family of fulgoromorph (planthopper), comprising of over 1500 species in over 170 genera (Holzinger et al., 2002). Drawn above is Oteana (source: Hoch (2006)).

It is accepted as being relatively basal in the Fulgoromorpha (Yeh & Yang, 1999), and the only thorough cladistic analysis to date has recovered it as monophyletic (Ceotto & Bourgoin, 2008), with the following combination of apomorphies; none of these are unique to the Cixiidae, but their combination is unique:

  • Flagelliform aedeagus;
  • Sixth and seventh abdominal sternites formed by two sclerites;
  • Six spines on the hind tibia’s apex;
  • Tubercles on the forewing veins.

However, there is a lot of resistance to the idea of a monophyletic Cixiidae, since the level of homoplasy is high enough to cause problems for morphological analyses (Ceotto & Bourgoin, 2008). A particularly problematic family with respect to the Cixiidae is the Achilixiidae, a family which some studies place inside the Cixiidae (Liang, 2001), a position rejected by other studies (Urban & Cryan, 2006). Ceotto et al. (2008) conducted a thorough molecular analysis that recovered the Cixiidae as paraphyletic, with the Delphacidae arising from within the family. While the exact relationships need more work, it is mostly accepted that the family is paraphyletic.

The current higher-level classification used is in need of revision, precisely because of this paraphyly (see the Ceotto et al. (2008) phylogeny above). They are typically divided into three subfamilies: the Bothriocerinae Muir 1923, Borystheninae Emeljanov 1989, and Cixiinae Spinola 1839.

I sometimes confuse them with cicadas in the field; they basically look like very small cicadas. You can distinguish them with the following characters, which will tell you that you’re looking at a fulgoromorph, not a cicada: the antennal pedicel is enlarged or bulbous, the mesothorax has tegulae, and the bases of the middle coxae are widely separated. So if you’re going to collect them, make sure you have a hand lens with you. They can be recognised as cixiids instead of other fulgoromorphs by their clear, membraneous wings (see opening drawing) held at a very low angle to the body. Females can be recognised by their immoveable tibial spur; the sword-shaped ovipositor is also easily-recognisable, but is also found in delphacids.

Interestingly, some cixiids have patterns on their wings, namely dark patterns at the rear of the wings (Scherbakov & Popov, 2002). These serve to distract a predator by making it think the rear of the wing is the head of the animal.

Adults can be found on the surface of plants, and it’s easy to distinguish the sexes. Females have a distinct sword-shaped ovipositor, using it to lay eggs either in the soil or in plant tissue. If you want to catch them passively, a Malaise trap set up to capture inter-plant movement is the best choice. If you want an estimation of predation pressure on them, you can check out bird droppings: their hindlegs are often found there, and are easily recognisable (Ralph et al., 1985).

Nymphs commonly live at the base of plants on the surface, or between the roots (they commonly have flattened tibiae, possibly as digging adaptations). Some may be found on fungi on rotten wood, or on ferns; some are even associated with ants. In all though, the nymphs are hard to see because of their cryptic colouration and habits. Host plants or specificity aren’t known. Nymphs are very hard to identify to species-level, so you’ll most likely want to capture them alive and rear them to adulthood for ID.

Mating involves using vibrational signals: males send messages, females reply (Mazzoni et al., 2010); this is a cooption of their regular way of communication. Copulation can be pretty interesting: Hoch & Remane (1985) describe how Hyalesthes males have to be upside down and the females the right side up facing the opposite direction (if we humans were to try it like this, then the woman would end up with the man’s feet in her face while penetration was happening); Sforza & Bourgoin (1998) describe how the partners copulate side-by-side while facing opposite directions (in other words, the male has to twist his genitalia considerably to get them in; I don’t want to think about the human equivalent).

They’re somewhat unique in being one of only 6 hemipteran families with troglobitic, cave-dwelling representatives (Romero, 2009), with 80% of the cave-dwelling Fulgoromorpha being cixiids. The most famous cases are the genera Solanaima and Undarana in Australia, and Oliarus in Hawaii. Solanaima especially is considered to be a model system for studying evolution in caves, as all transitional stages are represented, from epigaean (surface-dwelling), to troglophilic (occasional cave-dwellers) to troglobitic (blind, flightless. unpigmented cave-dwellers) (Hoch & Howarth, 1989). Oliarus is also intensely studied, but more in relation to the time-scale involved in cavernicolous evolution. These species have independently moved into lava tubes, habitats whose formations can be precisely dated geologically, and study of them can yield important information about how fast features can be lost (Hoch & Howarth, 1999).

They’re also unique in being one of the few fulgoromorphs known to act as vectors for plant viruses and bacteria (Nault & Ammar, 1989), e.g. Hyalesthes obsoletus transmitting stolbur phytoplasmas (phloem-dwelling pathogenic bacteria) on grapevines (Maixner et al., 1995), the cause of what’s known as Vergilbungskrankheit (German-speaking wine-growing areas), Bois noir (French), or Legno nero (Italian), a disease that leads to shrivelled grapes, downward-rolling leaves, and lack of lignified shoots. Needless to say, it’s a huge harm to for any wine production, sometimes with over 50% of vines becoming infected during an epidemic, so research into associated cixiids is pretty active. The transmission is completely accidental, there is no manipulation by the phytoplasma. The larvae acquire them while feeding on stinging nettle roots, and they’re transmitted by the adults to the grapevine when they pierce the grapevine to suck the phloem out (similar to how mosquitoes inject malaria into us). The grapevine is a dead-end host for the phytoplasma.

Another disease transmitted by a cixiid, Haplaxius crudus (still often erroneously referred to as Myndus crudus due to general ignorance of taxonomy; New World Myndus were placed in Haplaxius by Emeljanov (1989)), is lethal yellowing, a disease of palm trees, very damaging in the Carribean region throughout this species’s range. Any infected palm is guaranteed to die: it’s single-handedly responsible for the elimination of coconut palms on the Carribean coast of central America. Several control methods have been tried, from standard insecticides (only good for preventing dispersal), to planting plants unsuitable for nymph growth, but the most successful way has simply been to plant different species of palm known to be more resistant to the disease; hopefully, this will lead to some sort of GM research to get their resistance-enabling genes into the more susceptible date- and coconut palms.

Besides those, they cause structural damage to plants by feeding (H. crudus is again implicated, but with sugarcane), but this is considered negligible relative to other pests.

Their fossil record is rather sparse, although they are one of the commonest groups found in Baltic amber (Szwedo et al., 2006); one is pictured above (Sczwedo & Sontag, 2009). As should be expected, the bulk of their record comes from ambers, specifically Dominican (e.g. Szwedo, 2000) and Baltic amber (Gębicki & Szwedo, 2000), as well as Lebanese amber (Szwedo, 2001). However, the oldest record comes in the form of ‘Cixius’ petrinus, preserved in real rock from the Early Cretaceous Weald Clay, UK (Fennah, 1961).

References:

Ceotto P & Bourgoin T. 2008. Insights into the phylogenetic relationships within Cixiidae (Hemiptera: Fulgoromorpha): cladistic analysis of a morphological dataset. Systematic Entomology 33, 484-500.

Ceotto P, Kergoat GJ, Rasplus J-Y & Bopurgoin T. 2008. Molecular phylogenetics of cixiid planthoppers (Hemiptera: Fulgoromorpha): New insights from combined analyses of mitochondrial and nuclear genes. Molecular Phylogenetics and Evolution 48, 667-678.

Emeljanov AF. 1989. On the problem of division of the family Cixiidae (Homoptera, Cicadina). Entomological Review 68, 54-67.

Fennah RG. 1961. The occurrence of a Cixiinae fulgoroid (Homoptera) in a Weald Clay. Annals and Magazine of Natural History 13, 161-163.

Gębicki C & Szwedo J. 2000. Kulikamia jantaris gen. et sp. n. from Baltic amber (Hemiptera: Fulogroidea: Cixiidae). Polskie Pismo Entomologisczne 69, 167-173.

Hoch H. 2006. New Cixiidae from Eastern Polynesia: Oteana gen.nov. and Manurevana gen. nov. (Hemiptera: Fulgoromorpha). Zootaxa 1209, 1-47.

Hoch H & Remane R. 1985. Evolution und Speziation der Zikaden-Gattung Hyalesthes Signoret, 1865 (Homoptera Auchenorrhyncha Fulgoroidea Cixiidae). Marburger entomologische Publikationen 2, 1-427.

Hoch H & Howarth FG. 1989. Six new cavernicolous cixiid planthoppers in the genus Solanaima from Australia (Homoptera: Fulgoroidea). Systematic Entomology 14, 377-402.

Hoch H & Howarth FG. 1999. Multiple cave invasions by species of the planthopper genus Oliarus in Hawaii (Homoptera: Fulgoroidea:Cixiidae). Zoological Journal of the Linnean Society 127, 453-475.

Holzinger W, Emeljanov AF & Kammer-Lander I. 2002. The family Cixiidae – A review. In: Holzinger W (ed.). Zikaden — Leafhoppers, Planthoppers and Cicadas (Insecta: Hemiptera: Auchenorrhyncha), Denisia 4.

Liang AP. 2001. Morphology of antennal sensilla in Achilixius sandakanensis Muir (Hemiptera: Fulgoromorpha: Achilixiidae) with comments on the phylogenetic position of the Achilixiidae. Raffles Bulletin of Zoology 49, 221-225.

Maixner M, Ahrens U & Seemüller E. 1995. Detection of the German grapevine yellows (Verglibungskrankheit) MLO in grapevine, alternative hosts and a vector by a specific PCR procedure. European Journal of Plant Pathology 101, 241-250.

Mazzoni V, Lucchi A, Ioriatti C, Virant-Doberlet M & Anfora G. 2010. Mating Behavior of Hyalesthes obsoletus (Hemiptera: Cixiidae). Annals of the Entomological Society of America 103, 813-822.

Nault LR & Ammar ED. 1989. Leafhopper and Planthopper Transmission of Plant Viruses. Annual Review of Entomology 34, 503-529.

Ralph CP, Nagata SE & Ralph CJ. 1985. Analysis of bird droppings to describe diets of small birds. Journal of Field Ornithology 56, 165-174.

Romero A. 2009. Cave Biology: Life in Darkness.

Scherbakov DE & Popov YA. 2002. Order Hemiptera Linné, 1758. The bugs, cicadas, plantlice, scale insects, etc. In: Rasnitsyn AP & Quicke DLJ (eds.). History of Insects.

Sforza R & Bourgoin T. 1998. Female genitalia and copulation of the planthopper Hyalesthes obsoletus Signoret (Hemiptera: Fulgoromorpha: Cixiidae). Annales de la Société entomologique de France (NS) 34, 63-70.

Szwedo J. 2000. Oliarus kulickae sp. n. from Dominican amber (Hemiptera: Fulgoroidea: Cixiidae). Polskie Pismo Entomologiczne 69, 161-166.

Szwedo J. 2001. A substitute name for the extinct genus Mundopoides Fennah (Hemiptera: Fulgoroidea: Cixiidae). Genus 12, 275.

Szwedo J & Sontag E. 2009. The traps of the “amber trap”. How inclusions could trap scientists with enigmas. Denisia 26, 155-169.

Szwedo J, Bourguin T & Lefebvre F. 2006. New Mnemosynini taxa (Hemiptera, Fulgoromorpha: Cixiidae) from the Palaeogene of France with notes on their early association with host plants. Zootaxa 1112, 31-41.

Urban JM & Cryan JR. 2006. Evolution of the planthoppers (Insecta: Hemiptera: Fulgoroidea). Molecular Phylogenetics and Evolution

Yeh WB & Yang CT. 1999. Fulgoromorpha phylogeny based on the 28S rDNA nucleotide sequence. Chinese Journal of Entomology 11, 87-111.

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