All new taxa reported here provide 40.6% of the total number of the identified winged aphids (216) from Tunisia. A number of 89 winged aphid taxa are recognized composed of 78 species, 8 at genus level and 3 subspecies recorded for the first time in the tunisian network. Nevertheless, 12 species were previously cited on host plants (Kamel-Ben Halima and Mdellel 2010; Kamel-Ben Halima 2012). For our knowledge, species as Aspidaphis adjuvans, Cryptaphis poae, Izyphia leegei, Myzocallis komareki, Paczoskia paczoskii, Patchiella reaumuri, and Rhopalosiphoninus sp. are identified for the first time in Tunisia and in the Maghreb region.
Species origin
The origin of the identified aphids is diverse and sometimes unknown. Some species are part of the Mediterranean aphidofauna: Aphis punicae, Cinara laportei (Euromediterranean oriental species cited from Morocco, Algeria, Turkey, Italy), Dysaphis foeniculus, Eulachnus tuberculostommatus, Forda formicaria and Geoica utricularia of Mediterranean origin, Macrosiphoniella absinthii, Melanaphis donacis and Protaphis sp. (Remaudière 1985; Millar 1990; Roberti 1990; Blackman and Eastop 2006). Species originated from Africa Aphis (Protaphis) pseudocardui and Uroleucon compositae. Other species from Europe as Acyrthosiphon loti, Amphorophora idaei, Aphis coronillae, Aphis craccae, Aphis frangulae, Aphis idaei, Aphis sambuci, Aphis schneideri, Brachycaudus prunicola, C. poae, Dysaphis apiifolia, I. leegei, Lachnus sp., Macrosiphum funestum, Macrosiphum gei, Myzus ascolanicus, M. komareki, Patchiella reaumuri, Pemphigus bursarius, Phorodon humuli, Sipha elegans, Tetraneura akinire, T. nigriabdominalis, Therioaphis riiehmi (Blackman and Eastop 2000; Mifsud 2008). Additional species are known from Asia as Acyrthosiphon kondoi, Brachycaudus prunicola, Hyperomyzus carduellinus, Melanaphis donacis, Greenidea ficicola and G. psidii, Myzus varians (native to China), Rhopalosiphoninus sp., Takecallis sp., and Aulacorthum circumflexum (from South East Asia seems most likely). Hyperomyzus carduellinus is an Asian species found from Afganistan to Korea and Taiwan. It was also cited from Australia and Africa. This aphid is specific to Sonchus (Halbert 1999) which is a common weed in Tunisia. Two Greenidae species reported here Greenidea fiscicola was first captured in 2006 (Boukhris-Bouhachem 2009) and Greenidea psidii in 2009, both known as fig tree and Ficus colonisers. Rhopalosiphoninus sp. originated from India, and the Far East. New species were also introduced from America, Aphis illinoisensis (native to America) was newly introduced to Tunisia in 2006 and considered as an invasive species on grape vine (Kamel-Ben Halima 2009). A. illinoisensis was recently reported as a newly established introduction to Europe and the Mediterranean basin, with records from southern Turkey, Greece, Israel, northern Cyprus, Algeria, Libya, Montenegro and Malta (Mifsud et al. 2011). Illinoia lambersi, Macrosiphum albifrons (widespread in North America), Moneliopsis caryae, Uroleucon ambrosiae (originated from Central, North and South America. Wahlgreniella nervata (Mexico, Western North America). M. caryae, North American species associated to juglandaceae, first recorded by the suction trap in 2010. Furthermore, species are world-wide with unknown or mystery origin, undoubtedly transported by men Aphis nasturtii, Aulacorthum circumflexum, Cinara tujafilina cosmopolitan, Coloradoa rufomaculata, Dysaphis tulipae, Myzus ornatus, M. ascolanicus (seems from America), Phorodon cannabis, P. humuli. Patchiella reaumuri has an apparently rather patchy distribution in Europe (England, Italy, Bulgaria and Turkey). It has also been recorded from various countries in South and South-east Asia and from North America and may be introduced from China (Kurosu et al. 2022). P. paczoskii is present in Europe (France, Rumania, Ukraine) described on stems and undersides of leaves of Echinops spp. Aspidaphis adjuvans is known from Europe and Asia, and North America, living cryptically on Polygonum aviculare, often at roadsides or on paths. Most new identified species are common with Italy (58 species based on Roberti paper in 1990) and with Turkey (48 species based on (Görür et al. 2012) probably linked to the intensive exchanges between our countries these last decades. Than we listed 31 species common with the neighbouring countries as Algeria based on (Laamari et al. 2009; Laamari et al. 2013). Other species newly shared with other countries 24, 12, 7 species from Europe, Asia and America respectively.
Species richness according to trap types
The suction trap added the most important number of new species compared to yellow traps even their total species abundance is less important. In contrast, yellow traps captured unique species not present in the suction trap. Some aphid species as Acyrthosiphon kondoi, Protaphis sp., A. illinoisensis and the subspecies A. f. cirsiiacanthoidis and A. f. solanella, seem not having a high flight level and were not often captured by the suction trap while they were frequent in yellow traps. Aspidaphis adjuvans Cryptaphis poae, Myzocallis komareki, Uroleucon ambrosiae, Uroleucon tussilaginis… were only captured by yellow traps. Furthermore, other species as G. ficicola, A. craccae and Paracletus donistorpei flight at high levels and were captured by the suction trap only. Species as T. nigriabdominalis, D. tulipae, D. foeniculus, T. akinire, H. carduellinus, D. apiifolia, U. compositae were regularly frequent in the three traps. This difference seems linked to the species flight behaviour (Dietzgen et al. 2016).
The species numbers and the annual average captures by yellow traps were higher than by suction trap were. Hence, a greater qualitative efficiency of the suction trap compared to the yellow traps, which appears clearly, if we consider the low density of winged aphids of the taxa that were taken (Seco Fernández et al. 1989). Furthermore, only suction traps indicates the number of aphids per unit volume of air and are non-selective, but water traps effectively catch those aphids that attracted to yellow. In some seed-potato growing countries, yellow water traps are considered as the most useful tools to monitor aphid flights. (Döring and Kirchner 2022) confirmed that yellow colour attracted the highest number of winged aphids and explained the yellow preference of aphids visually guided in host finding behaviour. On the other hand, some consider the use of yellow water traps complementary to that of suction traps, depending on the aphid species to be caught (Robert et al. 1987). Hence, if the number of capture is observed, the suction trap is by far the most effective trap since it captured a lot of insects in a very short period (Devigne and de Biseau 2014; Bărăscu 2021). The results suggest that not only one trap is able to catch all aphid species while a combination of both methods is more informative and can improve monitoring of aphid biodiversity.
Suction traps and YWTs are regularly used for monitoring aphid abundance. The 12.2 m high Rothamsted suction trap provides information about the composition and long distance movement of aphid taxa in large areas and helps to recognise an overall increase in the risk of virus transmission (Taylor 1986). YWT may be important for aphid control programmes where monitoring of aphids in the field informs the threshold risk level of virus transmission and the moment to begin measures for control of aphids (Döring and Kirchner 2022).
Species abundance
The most commonly species were classified by their abundance, Dysaphis tulipae, T. nigriabdominalis, D. foeniculus, Tetraneura akinire, D. apiifolia, Hyperomyzus carduellinus, Uromelan sp., Uroleucon compositae, Protaphis sp., Aphis fabae cirsiiacantoidis; these species/subspecies occurred in large numbers in YWTs but only few individuals of these species were caught within the suction trap. These differences may be associated with their activity and the height at which the species are normally flying (Kirchner et al. 2013).
With less frequency D. devecta, A. fabae solanella, A. illinoisensis, Amphorophora idaei, Paracletus donisthorpei, Acyrthosiphon kondoi, Melanaphis donacis, Aphis craccae, Macrosiphoniella abrotani, Greenidea psidii, Aphis frangulae, Greenidea ficicola. The other species are occasional as F. formicaria, M. ornatus, Macrosiphum albifrons, Iziphia sp., M. elizabethae, M. komareki, W. ossiannilssoni, B. prunicola, C. tujafilina, H. eryngii, M. persequens, Macrosiphoniella sp., M. albidum, U. aeneum, W. nervata… Other species were rarely captured as Aphis coronillae, A. ilicis, A. nasturtii, A. schneideri, A. adjuvans, C. populeti, C. poae…
Landscape richness impact
The diversity and abundance of aphids depends on the landscape composition. In fact, the distribution of aphids in the region is determined by the availability of host plants and has been strongly affected by agricultural practices (Foottit and Maw 2014; Holland et al. 2021). Traps were located in agricultural areas inside farms. The predominance of Aphidinae may be explained by the trap position and surrounding cultures. This subfamily includes the majority of agricultural aphid pest species as well as of species colonizing wild flora (either herbs or shrubs). However, forest species are the second abundant ones probably because YWT of Douala is near the forest of Korbous. D. tulipae was the most abundant aphids in the traps. It occur on many monocots including Arum, Chionodoxia, Crocus, Freesia, Gladiolus, Iris, Lilium, Moraea, Musa, Scilla and Strelitzia, colonising shoots and leaves of growing plants, and on underground stems and bulbs. It is probably cultivated in the nearby nurseries. Tetraneura nigriabdominalis occur on roots of Gramineae as Cynodon, Digitaria, Echinochloa, Oryza, Saccharum, Setaria. It made galls on various Ulmus spp. in East Asia, South and East Europe and USA (Blackman and Eastop 1994). Dysaphis apiifolia form dense colonies at leaf bases of various Umbelliferae (Anethum, Ammi, Apium, Conium, Foeniculum, Laserpitium, Levisticum, Petroselinum, Peucedanum, Ptychotis, Smyrnium). It is a world-wide pest of celery and parsley (Blackman and Eastop 2000). It occurs in Middle East, Central Asia, Africa, Mauritius, Australia, North and South America, and is mostly anholocyclic, but may be partially heterocyclic/hololocyclic in the Mediterranean basin. Hyperomyzus carduellinus occur on various Compositae (Gynura, Ixeridium, Lactuca, Prenanthes, Reichardia, Senecio, Sonchus, Taraxacum, Tridax). In southern Africa, India, Japan, Korea, SE Asia, Australia, New Zealand, Fiji, and recorded from Florida. Uroleucon compositae a very polyphagous species occuring on Compositae is a pest of safflower. It is widely distributed in Africa and on the Indian subcontinent. Protaphis sp., is reported from Artemisia sp., Cirsium spp., Chamaemelum, Cichorium, Helichrysum, Eryngium, Inula, Pulicaria… Aphis fabae cirsiiacantoidis occur on Cirsium arvense, which is common plant in Tunisia. Hence, species richness is the result of environmental factors, historical factors and species interactions within the species assemblage (Gaston 2000; Whittaker and Fernández-Palacios 2007; Bachmann et al. 2014). Several study have proved a positive correlation between habitat heterogeneity and richness (Tews et al. 2004). The distribution of aphids in the region was determined by the availability of host plants and has been strongly affected by agricultural practices (Foottit and Maw 2014). Weeds may affect the ability of dispersing insects to locate crop plants. The host relationship between insects and plants is highly variable, ranging from very specialized to generalized feeding behaviours (Capinera 2005). It has also shown the aphid-species richness was related to the variation of the human population in European countries. A positive correlation was found between the concentration of the number of people in urban areas and the number of aphid species (Pautasso and Powell 2009).
Virus vectors
Various Aphidinae species are vectors of virus diseases on crops or trees (e.g. Aphis spiraecola, Myzus persicae, Aphis gossypii, Aphis fabae, Dysaphis plantaginea, Aphis illinoisensis). Because aphids transmit the virus most damaging to potato seeds production, Potato virus Y (PVY), we speculate that the distribution of aphids may determine the level of infections. The importance of aphid species in the epidemiology of non-persistent viruses in Tunisia has highlighted in several studies (Boukhris-Bouhachem et al. 2007; 2011). Our study identified new aphids already known to be vectors of PVY (Ragsdale et al. 2001), as Aphis nasturtii, Aulacorthum circomflexum, Dysaphis species, Metopolophium albidum, Myzus ligustri, Phorodon humuli, and Uroleucon species. It would be interesting to test their transmission capacity in order to evaluate their possible role in the epidemiology of PVY in Tunisia. Furthermore, among these new aphids there are also vectors of other diseases on crops and trees: Aphis nasturtii, A. illinoisensis, A. craccae, A. idaei, Amphorophora idaei, A. rubi, Myzus ascolanicus, M. ornatus, Phorodon cannabis, Uroleucon compositae. This will increase probably the virus numbers and propagation in Tunisia. The risk of virus transmission by an increase in aphid vector numbers can be reduced through adjustment of planting and harvesting dates to avoid peak vector activity which is region specific (Krüger and Waals 2020).
- A. kondoi is a native of Asia, where it occurs from India to Japan, spread and is established in South Africa, Middle East and South American countries (Blackman and Eastop 1984) . A. kondoi, is reported as a vector of bean yellow mosaic virus a potyvirus (Chan et al. 1991).
- A. nasturtii is sub-cosmopolitan species and is an efficient vector for the non-persistent potato A Potyvirus, potato Y Potyvirus, and aucuba mosaic Potexvirus, but a poor vector of potato leafroll Luteovirus (Dietzgen et al. 2016). This aphid found throughout Europe, Malta, Middle East, Northern India, Pakistan and Japan, and introduced into North America, Chile, Ethiopia, Kenya and South Africa. His primary host is Rhamnus spp., especially R. cathartica, but it is polyphagous on a wide range of secondary herbaceous hosts, such as Rumex spp., Solanum tuberosum, and Veronica beccabunga (Blackman and Eastop 2006).
- Amphorophora idaei originated to Europe is a vector of raspberry mosaic virus and raspberry leaf spot (Blackman and Eastop 1984).
- Aphis craccae occurring throughout Europe, also in Japan and China and introduced in North America and can transmit bean yellow mosaic and cucumber mosaic virus.
- Aphis idaei, throughout Europe, east to Ukraine, New Zealand. It is a vector of raspberry vein chlorosis and rubus yellow net.
- Aphis schneideri, originated from Europe and vector of gooseberry vein banding virus.
- Aulacorthum circumflexum, probably from Asia, is able to transmit more than 30 viruses (e.g. barley yellow dwarf virus, potato leaf roll, …) and on ornamentals, mosaic virus, primula mosaic virus and tulip breaking virus (Alford 2012) and vector of the chrysanthemum viruses (Miller and Stoetzel 1997).
- Dysaphis apiifolia is found in Europe, the Middle East, Central Asia, Africa, Mauritius, Australia, and North and South America. D. apiifolia is a worldwide pest on celery and parsley, and transmits celery mosaic potyvirus (Blackman and Eastop 2000).
- Dysaphis tulipae, cosmopolitan and vector of the persistent lily virus and non-persistent tulip breaking virus.
- Illinoia lambersi seems to be introduced from North America to Europe and South America; it feed on numerous Rhododendron. It may also vector non-persistently transmitted plant viruses.
- M. ascolanicus of mystery origin is a vector of about 20 plant viruses in Europe, India, Pakistan, Japan, Australia, New Zealand, Antipodes, Auckland Isles, North and South America (CABI 2017). Proven to be vector of about 20 plant viruses (beet mosaic, beet yellows, cucumber mosaic virus, onion yellow dwarf, potato virus Y).
- M. varians, native to China and recorded also from Japan, Korea, Taiwan and Thailand, Europe, America; it is vector of plum pox virus.
- Myzus ornatus, throughout the world, able to transmit at least 20 plant viruses (potato leaf roll, Malva yellows, pea enation mosaic …)
- Phorodon cannabis, vector of cannabis streak virus in central and southern Europe, Asia, North Africa, North America (Blackman and Eastop 1984).
- Phorodon humili, vector of hop mosaic, arabis mosaic, plum pox virus; throughout Europe, Central Asia, North Africa, South Africa.
- Uroleucon compositae is recorded as a vector of passion fruit woodiness virus (Blackman and Eastop 1984).
Obviously, the best-known species are those of greatest importance as vectors. Nevertheless, it is possible that some little-known aphid to spread around become a major pest with climate changes or landscape variations.