InfluentialPoints.com
Biology, images, analysis, design...
Aphids Find them How to ID AphidBlog
"It has long been an axiom of mine that the little things are infinitely the most important" (Sherlock Holmes)

 

 

Identification & Distribution

On the primary host (Pistacia), Smynthurodes betae fundatrices induce small red midrib galls, and their offspring induce yellow-green or red spindle-shaped leaf margin galls. On the secondary host (roots of many plants) adult apterae are small to medium-sized, globular in shape, and coloured a dirty yellowish white (see first picture below). They are wax dusted, and clothed with numerous fine hairs. Their immatures are light green (see second picture below). The head, prothorax, antennae and legs are light brown. The antenna are 5-segmented (cf. Trama  species which have six antennal segments) and the second antennal segment is elongated and about the same thickness as the third antennal segment. There are thick sclerotized rims on the primary rhinaria of the last two antennal segments. There are no siphunculi (cf. Protrama Tetraneura  and Anoecia  species, which have siphunculi). The body length of the adult Smynthurodes betae aptera is 1.6-2.7 mm.

Alates of Smynthurodes betae (see second picture below) have dark transverse bars on the abdominal tergites.

Clarified mounted  aptera and alate courtesy Favret, C. & G.L. Miller, AphID.  Identification Technology Program, CPHST, PPQ, APHIS, USDA; Fort Collins, CO.

Where the primary host (Pistacia) is found, the bean root aphid goes through its full life cycle, host alternating from Pistacia to numerous secondary hosts, especially in the Asteraceae, Fabaceae and Solenaceae. Smynthurodes betae can also persist on its secondary hosts as anholocyclic parthenogenetic populations. It commonly overwinters in ant's nests. Anholocyclic parthenogenetic populations of Smynthurodes betae are found in most countries of the world, except the coldest parts. It goes through its full life cycle in North Africa, Israel, Syria, Iran, southern Crimea, Transcaucasus and Pakistan.

 

Biology & Ecology

On the primary host

The primary host of Smynthurodes betae is largely the Mt Atlas mastic tree (Pistacia atlantica). The fundatrix, which develops from the egg, forms a small 5-7 mm long red gall on the midrib of the leaflet. The apterous second generation nymphs disperse from the fundatrix gall and induce the final, spindle-shaped galls about 20 mm long on the leaflet margin. Each final gall is formed by a single F2 (second generation) aphid.

Wool & Burstein (1991)  looked at the population ecology and evolutionary aspects of Smynthurodes betae in Israel. One aspect considered was the evolution and possible selective advantages of the two-gall life history strategy in the Fordinae. In the life cycle of Smynthurodes betae there are two colonization events: F2 apterae disperse away from the fundatrix galls, and F4 (fourth generation) alates disperse to the secondary hosts. Wool & Burstein suggest that the primitive life cycle involved a single fundatrix gall, and F2 aphids acquired the ability to form galls only later in their evolution. This is supported by the following facts:

  1. In most Pemphigidae only the fundatrix forms the gall.
  2. The entire life cycle of Smynthurodes betae on Pistacia atlantica can still be completed in some fundatrix galls.
  3. While the fundatrix galls of the five different species of Fordini are morphologically similar, the final galls are very different in structure and morphology.

There appears to be no advantage to the two-gall system in terms of total reproductive output since the two-gall root aphid Smynthurodes betae and the one-gall root aphid Aploneura lentisci produce similar numbers of offspring expressed per fundatrix. Instead the main advantage of the two-gall system was thought to be that clone subdivision spreads the risk of clone destruction by environmental factors or by natural enemies.

Inbar (1998)  investigated competition, territoriality and maternal defense in Smynthurodes betae. Videotaped behavior and experiments demonstrated that first instar offspring of the fundatrix protect their galling sites against competitors of their own species (the larger individuals win), as well as against first instar competitors of the sympatric galling aphid Forda riccobonii. In mature galls, adult aphids also protect their gall and their offspring from conspecific invaders and natural enemies. The fighting behavior of the adult aphid is unique: the aphid seizes the intruder while lying on its back, enabling use of all six legs and the mouthparts. Although the aggressive behavior of the adult aphid protects the gall and offspring, no distinct parental care behavior was observed. The territoriality and aggression are highly adaptive because of the limited number of galling sites. Under natural conditions, removal of the adult aphids from the galls resulted in significantly increased invasion by conspecific intruders. The results indicated that the role of interspecific competition and natural enemies in shaping adult behavior is rather limited. The open galls and the unique life-cycle of Smynthurodes betae encourage and prolong intraspecific competition and facilitate confrontations between adults and invading nymphs. The ability of the adult owner of a gall to prevent invasions of nymphs has promoted the evolution of maternal defense in this aphid. This study supported the hypothesis that galls, as high value resources that combine food and shelter, are often associated with defensive and social behavior.

Wool & Burstein (1991)  reported on parasitoids of Smynthurodes betae in Israel. They found that more than 20% of the fundatrix galls were parasitized by Monoctonia pistaciaecola. This was a new host record for this parasitoid. A pteromalid hyper-parasite was identified as Pachyneuron? leucopiscida. It was noted that rather few parasitoids are known from gall-forming aphids, compared with free-living ones.

On the secondary host

As is common for root aphids, rather less work has been done on Smynthurodes betae on their secondary host - the roots of beans, parsnip, Euphorbia species and Galium species - than on the primary host, despite the fact that Smynthurodes betae is more of a pest on the secondary than on the primary host. The picture below shows two white adult Smynthurodes betae (bean root aphid) on parsnip, one of them being transported in the jaws of a yellow meadow ant (Lasius flavus).

Image above by permission, copyright Maria Fremlin,  all rights reserved.

On its secondary host Smynthurodes betae is invariably attended by ants, and has been described as being entirely dependent on ants. The aphids we observed were very closely attended by Lasius flavus.

These ants would frequently pick up the aphids in their jaws (see picture below) and reposition them at less exposed places on the parsnip root.

Landis (1967)  noted that most root aphids are more or less dependent upon a few species of ants for survival. He studied the attendance of Smynthurodes betae by a thief ant (Solenopsis molesta) and the pavement ant (Tetramorium caespitum).

 

Other aphids on same host:

Primary hosts

Blackman & Eastop  list Smynthurodes betae on 4 Pistacia species: Pistacia atlantica (a pistachio tree species, Mount Atlas mastic tree, Persian turpentine tree), Pistacia mutica (wild pistachio tree), Pistacia terebinthus (turpentine tree, terebinth) and Pistacia vera (commercially-grown edible pistachio).

  • Blackman & Eastop list 13 species of aphid as feeding on Mount Atlas mastic tree (Pistacia atlantica) worldwide, and provide formal identification keys.

    Of those aphid species, Baker (2015)  lists 3 as occurring in Britain: Forda formicaria,  Forda marginata  and Smynthurodes betae.

  • Blackman & Eastop list 8 species of aphid as feeding on edible pistachio (Pistacia vera) worldwide, and provide formal identification keys.

    Of those aphid species, Baker (2015)  lists 4 as occurring in Britain: Forda marginata.  Geoica utricularia, Paracletus cimiciformis and Smynthurodes betae.

 

Damage and control

In the USA Smynthurodes betae may cause serious injury to seedling cotton plants at times in the coastal plains of the Carolinas, and to squash in Utah.

Acknowledgements

We are extremely grateful to Maria Fremlin  who sent us living specimens of Smynthurodes betae from colonies she found on parsnip roots in allotments in Colchester, Essex. Maria also provided the image of live adult Smynthurodes betae on parsnip root, shown above.

We have made provisional identifications from high resolution photos of living specimens, along with host plant identity. In the great majority of cases, identifications have been confirmed by microscopic examination of preserved specimens. We have used the keys and species accounts of Blackman & Eastop (1994)  and Blackman & Eastop (2006)  supplemented with Blackman (1974) , Stroyan (1977) , Stroyan (1984) , Blackman & Eastop (1984) , Heie (1980-1995) , Dixon & Thieme (2007)  and Blackman (2010) . We fully acknowledge these authors as the source for the (summarized) taxonomic information we have presented. Any errors in identification or information are ours alone, and we would be very grateful for any corrections. For assistance on the terms used for aphid morphology we suggest the figure  provided by Blackman & Eastop (2006).

Useful weblinks 

References

  • Inbar, M. (1998). Competition, territoriality and maternal defense in a gall-forming aphid. Ethology Ecology & Evolution 10, 159-170. Full text 

  • Landis, B.J. (1967). Attendance of Smynthurodes betae (Homoptera: Aphididae) by Solenopsis molesta and Tetramorium caespitum (Hymenoptera: Formicidae). Annals of the Entomological Society of America 60(3), 707. Abstract 

  • Wool, D. & M. Burstein, M. (1991). Parasitoids of the gall-forming aphid Smynthurodes betae [Aphidoidea: Fordinae] in Israel. Entomophaga 36(4), 531-538. Abstract 

  • Wool, D. & M. Burstein, M. (1991). A galling aphid with extra life-cycle complexity: population ecology and evolutionary considerations. Researches on population ecology 33(2) 307-322. Full text