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Oleander aphid, Milkweed aphidOn this page: Identification & Distribution Biology & Ecology: Life cycle Colour and aposematism Population dynamics Natural enemies Other aphids on the same host
Identification & Distribution
Adult apterae and immatures of Aphis nerii are bright yellow-orange or lemon-yellow, with dark antennae. The pictures below show live immatures on one of their prefered hosts, milkweed (an Asclepias species).
Both images copyright Alan Outen, all rights reserved.
Identification characteristics refer to adult Aphis nerii apterae (see first picture below). The antennal terminal process is 3.4-4.7 times the length of the base of the sixth antennal segment. The abdominal dorsum is entirely membranous. The legs including the hind tibiae are dark (cf. Aphis asclepiadis and several polyphagous Aphis species which have the hind tibiae pale for more than half their length). The rather long siphunculi and finger-shaped cauda are black, and the siphunculi are 1.7 - 2.7 times as long as the cauda. The body length of adult Aphis nerii apterae is 1.3-1.7 mm.
Aphis nerii is a specialized feeder on oleander (Nerium oleander), but may occur on other Apocynaceae species - especially Dregea sinensis and milkweeds (Asclepidaceae) where it forms large colonies on growing shoots and along midribs of leaves. Aphis nerii is regarded as polyphagous: It has been reported feeding on 16 other plant families, including the Asteraceae, Convolvulaceae and Euphorbiaceae - albeit sometimes as overflow hosts. It is anholocyclic virtually everywhere except, perhaps, Japan. Aphis nerii is distributed more or less worldwide in warmer climates. It is also found in protected environments (glasshouses) in temperate countries, and occasionally 'in the field'.
Biology & Ecology
Groeters & Dingle (1989) looked at the cost of being able to fly for Aphis nerii. Winged aphids begin reproducing about 1.5 days after wingless aphids. The longer maturation period is primarily due to slower development. Aphids destined to become winged adults underwent their final moult (=eclosion) after wingless aphids begin reproducing. The delay is not due to a post-eclosion, pre-reproductive flight since, beginning with the fourth instar, larval winged aphids were reared at a density of one per plant and the vast majority were not stimulated to fly under such low-density conditions. Thus, the ability to fly incurs a fitness cost in terms of delayed reproduction, irrespective of whether flight actually occurs. We did not observe a difference between morphs for lifetime fecundity, even though wingless aphids have larger abdomens than winged aphids and for both morphs there is a significant correlation between abdomen width and fecundity. Offspring produced by wingless aphids over the first four days of reproduction are larger than those produced by winged aphids, and the size difference at birth is maintained into adulthood. However, there are no differences in life history traits between these offspring, including maturation period and lifetime fecundity. Thus, reduced body size does not increase the cost of being able to fly, at least under the conditions of these experiments. The cost of being able to fly in this species should favour reduced production of winged individuals in populations that exploit more permanent host plants.
Image copyright Alan Outen, all rights reserved.
Colour and aposematism
Aphis nerii is often given as an example of an aposematic insect which is warningly coloured and contains toxic chemicals (e.g. Crawley (ed), 1992). Rothschild (1970) found cardiac glycosides in the aposematic aphid Aphis nerii fed on both Nerium oleander and Asclepias curassavica. The absence of oleandrin and calactin in the body tissues of this insect suggests they are absent from the phloem on which the aphids are believed to feed.
Host-specialized herbivores has long been hypothesized to be highly tolerant of, and sometimes sequestering, plant secondary compounds. Plant variation in secondary compounds should thus play an important and predictable role in shaping the performance and distribution of insect communities. Zust & Agrawal (2015) compared the performance of four naturally occurring aphid species on twenty different genotypes of the common milkweed Asclepias syriaca. Diet breadths of the four aphids ranged from broadly generalized (Myzus persicae) to a broad specialist with >50 hosts (Aphis nerii) to a narrow specialist with <10 hosts (Aphis asclepiadis) to monophagous (Myzocallis asclepiadis) which only feed on Asclepias (milkweed) species. Aphis nerii (all stages bright yellow-orange) and Myzocallis asclepiadis (ovipara yellow and black) can both be considered to have aposematic coloration.
Genotypes of milkweed consistently differed in functional traits such as concentrations of toxic cardenolides. The two more generalized species of aphids had the highest population growth rate overall, while growth rates decreased with increasing specialization. In contrast, honeydew exudation as a measure of phloem consumption increased with specialization; thus, resource-use efficiency was lower in specialist aphids. The two more generalized aphids grew best on genotypes with the highest plant growth rate (as an approximation for resource availability), while specialist aphids were not affected by plant growth. All four species contained apolar cardenolides in their bodies and excreted polar cardenolides, but only the most specialized aphid (Myzocallis asclepiadis) was negatively affected by increasing cardenolide concentrations of the host plant. Sequestration of cardenolides increased with diet specialization, with Myzocallis asclepiadis accumulating twice as much as any other species, perhaps explaining its susceptibility to plant cardenolides. Heritable plant traits differentially impacted co-occurring insect herbivores within the same guild. Generalist aphids were susceptible to variation in plant vigour but not defensive compounds. Increased host specialization resulted in lower resource-use efficiency, increased phloem throughput and ultimately higher cardenolide sequestration. Variation in these traits is thus likely to determine the relative distribution of generalist and specialist herbivores on plants in natural communities (see also Smith et al., 2008 and Bukovinszky et al., 2014).
Malcolm (1986) gives the case for kin selection being involved in the evolution of aposematism in Aphis nerii. He describes the influence on predator behaviour, and the survival of the aposematic Aphis nerii, in comparison with the palatable, cryptic aphid, Acyrthosiphon pisum, when offered to two predators with different foraging tactics. The experiments were designed to test Fisher's (1930) suggestion that aposematism could evolve by kin selection, since aposematic animals often occur in aggregations of relatives. Initially, spiders (Zygiella x-notata) and birds (Parus major) killed high proportions of the distasteful aphids (60% and 54% respectively). With experience, the predators killed and ate fewer Aphis nerii. The decreasing mortality of Aphis nerii after initial encounters with predators, coupled with its apparently obligate parthenogenesis, indicate that the evolution of aposematism in this soft-bodied insect is consistent with kin selection.
Groeters (1970) sampled populations of Aphis nerii in California, Iowa and Puerto Rico. Among these localities the aphid's host plants differ greatly in permanence. They compared populations for migratory potential, measured as the proportion of winged offspring produced in response to being crowded, and for life history and morphometric traits of the subsequent adult winged aphids. A negative correlation was predicted between degree of host plant permanence and migratory potential. As predicted, aphids from Iowa, where migration on to temporary hosts must occur each year, produce a greater proportion of winged offspring (37.7%) than those from California (25.7%) or Puerto Rico (31.6%) where hosts are more permanent. However, hosts in Puerto Rico appear to be more permanent than those in California, yet the difference between populations for migratory potential was opposite to that predicted. Within California the prediction again held: aphids collected from the most impermanent sites produce the greatest proportion of winged offspring. There were no population differences for any life history or morphometric traits of winged aphids that are important contributors to fitness or migratory ability such as time to reproductive maturity, fecundity or wing length. Nor did any traits covary with migratory potential. Thus, there does not appear to be an association of life history and morphology with migratory potential that could enhance the colonizing ability of migrant aphids. Groeters was unable to detect population differentiation for life history and morphology even though there is ample genetic variation within populations on which selection could act and an absence of constraints arising from genetic correlations that could prevent appropriate evolution of traits within populations. The exploitation of temporary host plants therefore occurs by an increase in the number of colonists produced and not by change in life history or morphology of those colonists.
Hall& Ehler (1980) looked at the population ecology of Aphis nerii on oleander in northern California. A native generalist, Lysiphlebus testaceipes, was the only primary parasitoid reared from Aphis nerii, and in certain cases, it was able to control the host population. However, parasitization by Lysiphlebus testaceipes was an inverse-density-dependent factor and thus not a significant mortality factor at high aphid population densities. The latter populations were apparently regulated through intraspecific mechanisms (e.g. competition). Outbreaks of Aphis nerii occurred only at urban sites where plants were regularly pruned and watered. These cultural practices resulted in an increased proportion of new, actively growing terminals (preferred by Aphis nerii) which led to increased density of aphids feeding on such terminals.
Agrawal et al. (2004) present experimental evidence for positive, negative, and no density dependence from 32 independent density manipulations of Aphis nerii in laboratory and field experiments. This substantial variation in intra- specific density dependence is associated with temperature and host-plant species. It is reported that as population growth rate increases, density dependence becomes more strongly negative, suggesting that the monotonic definition of density dependence used in many common population models is appropriate for these aphids, and that population growth rate and carrying capacity are not directly proportional. For populations that conform to these assumptions, population growth rate may be widely applicable as a predictor of the strength of density dependence.
Image copyright Alan Outen, all rights reserved.
Zehnder (2007) compared maternal effects and current environment on vital rates (birth rate, death rate, and movement rate) of Aphis nerii. Non-Mendelian maternal effects, the effects of maternal phenotype or environment on offspring phenotype, have been documented in numerous taxa. By affecting offspring vital rates, maternal effects have the potential to influence population dynamics. However, relatively few studies have directly linked maternal phenotype or environment to offspring vital rates. Additionally, even fewer studies have compared the magnitude of across-generation effects (i.e. maternal effects) to within-generation effects. Because of their telescoping of generations, aphids can be strongly influenced by maternal effects. The effects of maternal density and maternal host-plant species on offspring survival, fecundity, and alate formation were investigated experimentally in Aphis nerii. Additionally, the relative strength of maternal effects were compared with those operating within a generation. Therefore, in another set of experiments, the effects of current density and host-plant species (within-generation effects) on aphid vital rates were examined. While maternal effects were present, within-generation effects were much stronger and more strongly influenced aphid vital rates. Within a generation, aphids exhibited density-dependent survival, fecundity, and alate formation - and these effects varied among host-plant species. Their results indicate that while maternal effects have the potential to affect population dynamics, this potential is not always met. Additionally, the current environment, not the environment of previous generations, more strongly impacts population dynamics.
Smith et al. (2008) investigated the role of several factors in promoting coexistence among the aphids Aphis nerii, Aphis asclepiadis, and Myzocallis asclepiadis that all specialize on common milkweed (Asclepias syriaca). Competitive exclusion is thought to occur when interspecific competition is stronger than intraspecific competition. Consequently, they investigated whether predators, mutualists, or resource quality affected the strength of intra- vs. interspecific competition among aphids in factorial manipulations of competition with exposure to predation, ants, and variable plant genotypes in three separate experiments. In the predation-competition experiment, predators reduced aphid per capita growth by 66%, but the strength of intra- and interspecific competition did not depend on predators. In the ants-competition experiment, ants reduced per capita growth of Aphis nerii and Myzocallis asclepiadis (neither of which were mutualists with ants) by approximately one-half. In so doing, ants ameliorated the negative effects of these competitors on ant-tended Aphis asclepiadis by two-thirds, representing a novel benefit of ant-aphid mutualism. Nevertheless, ants alone did not explain the persistence of competitively inferior Aphis asclepiadis as, even in the presence of ants, interspecific competition remained stronger than intraspecific competition. In the plant genotype-competition experiment, both Aphis asclepiadis and Myzocallis asclepiadis were competitively inferior to Aphis nerii, with the strength of interspecific competition exceeding that of intraspecific competition by 83% and 23%, respectively. Yet these effects differed among milkweed genotypes, and there were one or more plant genotypes for each aphid species where coexistence was predicted. A synthesis of their results showed that predators play little or no role in preferentially suppressing competitively dominant Aphis nerii. Nonetheless, Aphis asclepiadis benefits from ants, and Aphis asclepiadis and Myzocallis asclepiadis may escape competitive exclusion by Aphis nerii on select milkweed genotypes. Taken as a whole, the coexistence of three host-specific aphid species sharing the same resource was promoted by the dual action of ants as antagonists and mutualists and by genetic diversity in the plant population itself.
Following its introduction into Europe, the common milkweed (Asclepias syriaca) has been free of most of the specialist herbivores present in its native North American range, except for the oleander aphid Aphis nerii. Bukovinszky et al. (2014) compared European and North American populations of Aphis nerii on European and North American milkweed populations to test the hypothesis that plant-insect interactions differ on the two continents. First, they tested if herbivore performance is higher on European plants than on North American plants, because the former have escaped most of their herbivores and have perhaps been selected for lower defence levels following introduction. Second, they compared two Aphis nerii lines (one from each continent) to test whether genotypic differences in the herbivore may influence species interactions in plant-herbivore communities in the context of species introductions. The North American population of Aphis nerii developed faster, had higher fecundity and attained higher population growth rates than the European population. There was no overall significant continental difference in aphid resistance between the plants. However, milkweed plants from Europe supported higher population growth rates and faster development of the North American line of Aphis nerii than plants from North America. In contrast, European aphids showed similar (low) performance across plant populations from both continents. In a second experiment, they examined how chewing herbivores indirectly mediate interactions between milkweeds and aphids. As specialist chewing herbivores of Asclepias syriaca are only present in North America, they expected plants from the two continents may affect aphid growth in different ways when they are challenged by a specialist chewing herbivore. They introduced monarch (Danaus plexippus) caterpillars onto milkweed plants from each continent and compared the resulting changes in plant quality upon European aphid performance. Caterpillar introduction decreased aphid developmental times on North American plants, but not on European plants, whereas fecundity and population growth rates were unaffected by induction on both plant populations. Their results show that genetic variation in the plants as well as in the herbivores can determine the outcome of plant-herbivore interactions.
Hartbauer (2011) looked at collective defense of Aphis nerii and Uroleucon hypochoeridis (Homoptera, Aphididae) against natural enemies. The main way aphids accomplish colony defense against natural enemies is a mutualistic relationship with ants, or the occurrence of a specialised soldier caste typical for eusocial aphids, or even both. Despite a group-living life style of those aphid species lacking these defense lines, communal defense against natural predators has not yet been observed there. Individuals of Aphis nerii and Uroleucon hypochoeridis (an aphid species feeding on Hypochoeris radicata) show a behavioral response to visual stimulation in the form of spinning or twitching, which is often accompanied by coordinated kicks executed with their hind legs. Interestingly, this behaviour is highly synchronized among members of a colony, and repetitive visual stimulation caused strong habituation. Observations of natural aphid colonies revealed that a collective twitching and kicking response was frequently evoked during oviposition attempts of the parasitoid wasp Aphidius colemani and during attacks of aphidophagous larvae. This response effectively interrupted oviposition attempts of this parasitoid wasp and even repelled this parasitoid from colonies after evoking consecutive responses. In contrast, solitary feeding Aphis nerii individuals were not able to successfully repel this parasitoid wasp. In addition, this response was also evoked through gentle substrate vibrations. Laser vibrometry of the substrate revealed twitching-associated vibrations that form a train of sharp acceleration peaks in the course of a response. This suggests that visual signals in combination with twitching-related substrate vibrations may play an important role in synchronising defense among members of a colony. In both aphid species collective defense in encounters with different natural enemies was executed in a stereotypical way and was similar to responses evoked through visual stimulation. This cooperative defense behavior provides an example of a surprising sociality that can be found in some aphid species that are not expected to be social at all.
Other aphids on same host: