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Saltmarsh aphids:

Living in a hazardous but productive environment

Staticobium staticis  Aphis tripolii  Dysaphis bonomii 

  <December 2014>  

Whilst outwardly unexciting, salt marshes are important to man. They shelter our coasts from erosion, filter pollutants & excess sediments & nutrients from the water, and support fisheries. Nonetheless, in developed countries, up to 80% of salt marsh has been lost to human development. Salt marshes are physically stressful habitats for both plants and animals, combining tidal flooding and high salinity. Salt marsh animals must tolerate or avoid alternating periods of submergence & emergence. Many have well-developed osmoregulatory mechanisms to deal with the highly variable salinity. Salt marsh dwellers also cope with natural disturbances by ice, floating debris, herbivores, fire, and sediments - which together play an important role in the dynamics of marsh plant communities.

Salt marshes can be extremely productive systems - their above-ground primary production often reaches 2000 g/m2/year. Saltmarsh was traditionally viewed as a detritus-based system, with this production going into detrital food chains instead of being consumed directly by herbivores,. This view, however, underestimated the importance of herbivores in saltmarsh community-structure. The most important insect herbivores are aphids and grasshoppers. Here we take a first look at aphids that successfully exploit salt marsh.

 

Sea lavender aphid (Staticobium staticis) - like its host, a saltmarsh specialist

Sussex is not well endowed with salt marsh, but Keyhaven in Hampshire gave us good numbers of that iconic salt marsh flower, the sea lavender (Limonium vulgare). This is a salt marsh specialist par excellence and typically form dense monospecific stands on marsh landscapes. It also grows on sea walls, where it is slightly easier to access and photograph (see below).

 

Whilst a variety of herbivores feed on sea lavender, it does have its own specific aphid: the sea lavender aphid (Staticobium staticis). Their adults (see below) can be either dirty-green or dirty-red with bicoloured siphunculi - the lower third brown and the upper parts black.

Foster (1984)  recorded very high densities (more than 50000 per square metre) of the sea lavender aphid on a salt marsh in Norfolk. The dense populations were in the middle of the marsh, with low numbers in the lower and upper zones of the marsh. We have only ever found small isolated colonies (see below) probably because the hazards of sloshing about in the middle of a salt marsh have kept us relatively close to its periphery!

Foster's study was mainly dedicated to 'disproving' a hypothesis put forward by Owen & Wiegert (1976)   who suggested that aphids could actually benefit their plant hosts. They proposed that honeydew excreted by the aphids acted as a carbohydrate source for soil-living, nitrogen-fixing bacteria, thus increasing the rate of nitrogen fixation - which would subsequently benefit vascular plants. Foster, however, demonstrated experimentally that the sea lavender aphid instead dramatically reduces the fitness of its host plant (as measured by its seed production) under natural conditions. Untreated heavily infested plants produced no seed at all whilst plants in plots that were treated with insecticide to kill the aphids set seed normally.

One example cannot of course 'disprove' a hypothesis, and Adam (1993)   pointed that the large dense single species populations of plants on saltmarshes are not typical of many natural systems, such as woodland. In this respect saltmarshes are more similar to agricultural monocrops, where we are all too-aware that aphids can greatly reduce plant fitness. Another weakness of Foster's study is the amount of honeydew reaching the salt marsh floor was not actually measured: much of it may have remained on the plant, or simply washed away... Owen & Wiegert's hypothesis has not gained many supporters in recent years.

Given the 'challenging' conditions on a saltmarsh, we would expect Staticobium staticis to show some clear morphological and physiological adaptations to its environment. One such modification is that the spiracles are covered by tubercle-like opercula. These apparently enable the aphids to survive several hours submergence in aerated seawater (Foster & Traherne, 1976 ) albeit nowhere near as long as the root feeding aphid Pemphigus trehernei - which can survive up to 20 days in aerated seawater!

 

Green sea aster aphid (Aphis tripolii) - a new rarity for Keyhaven Marshes

The sea aster (Tripolium pannonicum) is another plant confined to salt marshes and estuaries. It has fleshy lanceolate leaves and purple ray floret flowers (see pictures below).

 

Tripolium pannonicum has several specialized aphids, one of which is the green sea aster aphid Aphis tripolii (a colony is shown in the second picture above). Aphis tripolii is not so colourful as the sea lavender aphid, clearly opting for cryptic  rather than aposematic colouration.  The adult aphid (see below) is apple green with a dusky head. Its siphunculi are yellowish with dusky apices, and its cauda is dusky.

Aphis tripolii feeds on the upper parts of the leaves and flowers of sea aster in coastal salt marshes or on mud flats in a few European countries including Britain. We have only found Aphis tripolii once - again by Keyhaven Marshes in southern England. This is a new record for Hampshire as it is previously only known from the coastal fringe from Kent round to Norfolk and in Wales.

It took us a long time to find Aphis tripolii. We searched an awful lot of large healthy sea aster plants, to no avail. The tendency to get aphids on stressed plants is well known,  and we finally found a colony on a lone, rather sad-looking plant growing on the sea wall (see first picture below). Hacker & Betness (1995)  found a similar preference among Uroleucon ambrosiae, an American species of saltmarsh aphid which lives on salt marsh elder (Iva frutescens), although in that case the apparent reason was because coccinellid predators favoured taller more productive plants.

 

Although it is not referred to in aphid ID keys, our photos (see second picture above) reveal Aphis tripolii nymphs have a faint dorsal pattern of wax powdered spots.

The green sea aster aphid, unlike the sea lavender aphid, is attended by ants - as can be seen in the first picture below. The ant shows a superficial resemblance to the common black ant (Lasius niger), but we would appreciate identification from anyone who is more 'up' on ants than we are.

 

There has been very little research done on Aphis tripolii. Foster & Treherne (1976)  observed that in a submerged colony, the only aphids that died were those that moulted whilst immersed. Also the winged adults (see second picture above) were unable to fly after submergence (which is hardly a great surprise).

 

Parsnip mealy gall aphid (Dysaphis bonomii) - a new rarity for Rye Harbour

We now move from Keyhaven in Hampshire to Rye Harbour in Sussex, another fantastic coastal nature reserve with an all-too-small area of salt marsh. Fortunately they have recently (re-)created a new saltmarsh (shown below) which already has interesting wildlife. (The blue object in its center is one of our tabanid survey  traps.)

We also move from the middle of the salt marsh, to its edge, where wild parsnip (Pastinaca sativa) often grows in abundance. Unlike the plants above, wild parsnip is host to over 20 aphid species.

Some of those 20 aphid species are very common, but the parsnip mealy gall aphid (Dysaphis bonomii (shown below) is not. It feeds on the basal parts of wild parsnip and is only known from southern England and a few European countries (Sweden, Germany, Austria and Italy). Whilst Dysaphis bonomii appears to be very rare, we have no way of knowing how rare (or common) it really is because aphids are so under-recorded.

Dysaphis bonomii is distinguished by the complete, dark, cross-bands on many or all of its abdominal tergites. Also the siphunculi are longer and narrower than in related species. The only references in research papers are a few observations of its occurrence on its host plant, parsnip (Pastinaca sativa).

 

The pinkish-grey nymphs (first picture above) were clustered at the junction between a lower leaf and the stem. They resemble those of several other Dysaphis species such as Dysaphis radicola (see our July blog ). The winged morph (alate) also has clearly marked black dorsal bands.

Postscript...

There are several other saltmarsh aphids that we'll be looking for in 2015, none of which so far appear to have been photographed alive. Two more aphids feed on sea aster: Macrosiphoniella asteris feeds on the stems, and Pemphigus treherni feeds on the roots. The latter aphid has some fascinating behavioural characteristics, one of them being that the young nymphs disperse by floating in sea water. Then there are some coastal grass feeders: Sipha littoralis is a dark green aphid found in the leaf sheaths of various coastal grasses such as saltmarsh-grass (Puccinellia) and cordgrass (Spartina ). Like other saltmarsh species, Sipha littoralis can survive tidal emergence. Atheroides brevicornis is a brownish to black aphid found in coastal habitats on saltmarsh-grass and red fescue (Festuca rubra).

So why 'hunt' for aphids?? 

Acknowledgements

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

  • Adam, P. (1993). Saltmarsh Ecology. Cambridge Studies in Ecology. Cambridge University Press.

  • Foster, W.A. (1984). The distribution of the sea-lavender aphid Staticobium staticis on a marine saltmarsh and its effect on host plant fitness. Oikos 42, 97-104. Full text 

  •  Foster, W.A. & Treherne, J.E. (1976). Insects of marine saltmarshes: problems and adaptations. In: Cheng, L. Ed. Marine Insects . North Holland Publishing Co.  Full text 

  • Foster, W.A. & Treherne, J.E. (1978). Dispersal mechanisms in an intertidal aphid. Journal of Animal Ecology 47(1), 205-217. Full text 

  •  Hacker, S.D. & Bertness, M.D. (1995). A herbivore paradox: why salt marsh aphids live on poor quality plants. The American Naturalist 145(2), 192-210.  Full text 

  • Owen, D.F. & Wiegert, R.G. (1976). Do consumers maximize plant fitness. Oikos 27, 488-492.  Full text