Costs and constraints in aphid-ant mutualism

While many studies have demonstrated that ants provide beneficial services to aphids, Bristow (Ant-plant interactions, Oxford University Press, Oxford, 104–119, 1991) first questioned why so few aphid species are ant-attended. Phylogenetic trees have demonstrated multiple gains and loss of ant-attendance in the course of aphid-ant interactions, implying that mutualisms easily form and dissolve. Several studies have reported the factors that influence the formation and maintenance of aphid-ant interactions. Examples include the physiological costs of ant attendance, competition for mutualistic ants, ant predation on aphids, the influence of host plants, and parasitoid wasps. Recent physiological techniques have also revealed the chemical component of aphid-ant mutualisms. The honeydew of ant-attended aphids contains melezitose (a trisaccharide), which has an important role in aphid-ant interactions. Studies of cuticular hydrocarbons on aphids and ants have clarified the underlying mechanisms of ant predation on aphids. Attending ants also reduce aphid dispersal ability, causing the formation of fragmented aphid populations with low genetic diversity in each population. The reduced aphid dispersal could be partly explained by higher wing loading and reduction of flight apparatus due to ant attendance. Whether ant attendance is associated with the range of host plants of aphids or genetic variation in microorganism in aphids remain to be explored.     

Ant benefits in a seed dispersal mutualism

Myrmecochorous plant seeds have nutrient rich appendages, elaiosomes, which induce some ant species to carry the seeds back to their nest where the elaiosome is consumed and the seed is discarded unharmed. The benefits to plants of dispersal of their seeds in this way have been well documented, but the benefits to the ants from consuming the elaiosomes have rarely been measured and are less clear. Ant benefits from myrmecochory were investigated in a laboratory experiment using the ant Myrmica ruginodis and seeds of Ulex species. To separate the effects of elaiosome consumption on the development of newly produced larvae versus existing larvae, ten ‘Queenright’ colonies containing a queen were compared to ten ‘Queenless’ colonies. Six measures of colony fitness over a complete annual cycle were taken: sexual production, larval weight and number, pupal weight and number, and worker survival. Queenless colonies fed with elaiosomes produced 100.0±29.3 (mean ± SE) of larvae compared to non-elaiosome fed colonies which produced 49.6±19.0; an increase of 102%. Larval weight increased in both Queenright and Queenless colonies. In colonies fed with elaiosomes, larvae weighed 1.02±0.1 mg, but in non-elaiosome fed colonies larvae weighed 0.69±0.1 mg; an increase of 48%. The food supplement provided by Ulex elaiosomes was trivial in energetic terms, under the conditions of an ample diet, suggesting that these effects might be due to the presence of essential nutrients. Chemical analysis of Ulex elaiosomes showed the presence of four essential fatty acids and four essential sterols for ants.     

Punishment and partner switching cause cooperative behaviour in a cleaning mutualism

What are the mechanisms that prevent partners from cheating in potentially cooperative interactions between unrelated individuals? The cleaner fish Labroides dimidiatus and client reef fish both benefit from an interaction as long as the cleaner eats ectoparasites. However, the cleaner fish prefers some client mucus, which constitutes cheating. Field observations suggested that clients control such cheating by using punishment (chasing the cleaner) or by switching partners (fleeing from the cleaner). Here, we tested experimentally whether such client behaviours result in cooperative cleaner fish. Cleaners were allowed to feed from Plexiglas plates containing prawn items and fish flake items. A lever attached to the plates allowed us to mimic the behaviours of clients. As cleaners showed a strong preference for prawn over flakes, we taught them that eating their preferred food would cause the plate to either chase them or to flee, while feeding on flakes had no negative consequences. We found a significant shift in cleaner fish foraging behaviour towards flake feeding after six learning trials. As punishment and terminating an interaction resulted in the cleaners feeding against their preferences in our experiment, we propose that the same behaviours in clients improve the service quality of cleaners under natural conditions.     

Costs of two non-mutualistic species in a yucca/yucca moth mutualism

Mutualisms often involve significant costs for participants. Costs are inflicted by mutualists themselves, as well as by associated, non-mutualistic species. These costs are rarely quantified, however, particularly the ones extrinsic to the pairwise interaction. We compare costs inflicted by an obligate mutualist pollinator and two common exploiters of an Arizona yucca over a 2-year period. The magnitude of seed damage from seed and fruit-feeding beetle larvae (Carpophilus longus, Nitidulidae) was similar to damage from the seed-eating larvae of Yucca schottii's pollinator moth Tegeticula yuccasella (Prodoxidae), averaging about 15 seeds destroyed per fruit in each case. The two seed predators usually fed within the same fruits, although rarely side by side. In contrast, the presence of fruit-galling moth larvae (Prodoxusy-inversus, Prodoxidae) appeared to benefit the yucca: individual Tegeticula destroyed only half as many seeds in galled fruits as they did in ungalled fruits. We discuss three general implications of these results. Firstly, the costs of non-mutualists to the two mutualistic partners are not necessarily parallel. Secondly, measurable costs of non-mutualists do not necessarily translate into an impact on the success of the mutualism itself, because they may be incurred after mutualistic activities take place. Finally, the costs of mutualists to each other can differ substantially depending on the presence or absence of non-mutualistic species. Received:17 July 1996 / Accepted:10 June 1997     

Adding biotic complexity alters the metabolic benefits of mutualism

Mutualism is ubiquitous in nature and plays an integral role in most communities. To predict the eco‐evolutionary dynamics of mutualism it is critical to extend classic pair‐wise analysis to include additional species. We investigated the effect of adding a third species to a pair‐wise mutualism in a spatially structured environment. We tested the hypotheses that selection for costly excretions in a focal population (i) decreases when an exploiter is added (ii) increases when a third mutualist is added relative to the pair‐wise scenario. We assayed the selection acting on Salmonella enterica when it exchanges methionine for carbon in an obligate mutualism with an auxotrophic Escherichia coli. A third bacterium, Methylobacterium extorquens, was then added and acted either as an exploiter of the carbon or third obligate mutualist depending on the nitrogen source. In the tripartite mutualism M. extorquens provided nitrogen to the other species. Contrary to our expectations, adding an exploiter increased selection for methionine excretion in S. enterica. Conversely, selection for cooperation was lower in the tripartite mutualism relative to the pair‐wise system. Genome‐scale metabolic models helped identify the mechanisms underlying these changes in selection. Our results highlight the utility of connecting metabolic mechanisms and eco‐evolutionary dynamics.     

Population dynamics and mutualism: functional responses of benefits and costs

We develop an approach for studying population dynamics resulting from mutualism by employing functional responses based on density-dependent benefits and costs. These functional responses express how the population growth rate of a mutualist is modified by the density of its partner. We present several possible dependencies of gross benefits and costs, and hence net effects, to a mutualist as functions of the density of its partner. Net effects to mutualists are likely a monotonically saturating or unimodal function of the density of their partner. We show that fundamental differences in the growth, limitation, and dynamics of a population can occur when net effects to that population change linearly, unimodally, or in a saturating fashion. We use the mutualism between senita cactus and its pollinating seed-eating moth as an example to show the influence of different benefit and cost functional responses on population dynamics and stability of mutualisms. We investigated two mechanisms that may alter this mutualism's functional responses: distribution of eggs among flowers and fruit abortion. Differences in how benefits and costs vary with density can alter the stability of this mutualism. In particular, fruit abortion may allow for a stable equilibrium where none could otherwise exist.     

Costs and benefits of polyandry in a sexually cannibalistic mantis

Mating with more than one male often provides direct or indirect benefits to female fitness but can also increase the chance of injury and death. Costs of mating are expected to increase linearly with increasing mating number. But how such costs interact with benefits to determine the net payoff of mating multiply is not well understood. Using the highly cannibalistic Springbok mantis, Miomantis caffra, a species where females are stabbed in the abdomen by males during violent premating struggles that males initiate to avoid being cannibalized, we took an experimental approach to assess the economics of polyandry under the risk of external, male-inflicted injury. We predicted that females that mate multiply would be more likely to show abdominal injuries, have higher prereproductive mortality, produce fewer offspring and be more likely to engage in pre-mating cannibalism to avoid unwanted matings. In line with our predictions, we found that the likelihood of abdominal injury was highest among females that mated at least once, and prereproductive death was highest among females that mated twice or three times. Virgin females completely avoided these costs and produced some offspring parthenogenetically but not enough to provide a net benefit. Although mating was better than not mating, there was no singularly optimal mating number: females that mated once and three times produced similarly high numbers of offspring from the first ootheca, which resulted in an intermediate trough in offspring production at two matings. We also found little evidence that cannibalism was deployed as a mate-avoidance strategy: females consistently attacked and consumed males regardless of how many times they mated or how long they were housed with males. Our results suggest the possibility of two distinct mating strategies in M. caffra, where females either mate at a lower frequency to minimize costs or at a higher frequency to maximize benefits. We discuss possible explanations for this bimodal pattern in offspring production.     

Costs and benefits of a community special care baby service

Between January 1981 and December 1986 3829 low birthweight (<2500 g) infants and 1980 other high risk infants were cared for at home after they were discharged from hospital by a specialist neonatal nursing service. Of the infants who were referred to this service, 720 (12%) weighed under 2000 g and 1919 (33%) under 2250 g at the time of discharge home. The infants were visited by the community neonatal sisters on an average of 11 occasions, but the number of visits varied from six to over 100 depending on the needs of the child and parents. There was close liaison with other community and hospital staff. Two hundred and thirty (4%) referred infants were readmitted to hospital while under the care of the specialist nursing service. In 1985 the cost of the service was £127 000, or £123 for each infant referred. Providing this specialist support at home allowed much earlier discharge of low birthweight infants from hospital. When compared with the cost of providing continuing inpatient neonatal care earlier discharge was estimated to have saved roughly £250 000 in 1985.Low birthweight infants have an increased risk of serious illness or death that extends beyond the neonatal period. Many are born to young and socially disadvantaged parents who can benefit from expert guidance and support at home. A community neonatal nursing service has advantages for high risk infants and their parents, is cost effective, and allows more efficient use of limited hospital resources.     

Cheating on a mutualism: indirect benefits of ant attendance to a coccidophagous coccinellid

Coccinellids (Coleoptera: Coccinellidae) are generally unable to prey on ant-tended prey. However, particular coccinellid species have morphological, behavioral, or chemical characteristics that render them immune to ant attacks, and some species are even restricted to ant-tending areas. The benefit gained from living in close association with ants can be twofold: (1) gaining access to high-density prey areas and (2) gaining enemy-free space. Here, the myrmecophily of Azya orbigera Mulsant (Coleoptera: Coccinellidae), an important predator of the green coffee scale, Coccus viridis (Green) (Hemiptera: Coccidae), is reported. In this paper, three main questions were studied. (1) Are the waxy filaments of A. orbigera larvae effective as defense against attacks of the mutualistic ant partner of C. viridis, Azteca instabilis F. Smith (Hymenoptera: Formicidae)? (2) Does A. instabilis reduce the rate at which A. orbigera larvae prey on scales? (3) Do A. orbigera larvae gain enemy-free space by living in close association with A. instabilis? Laboratory and field experiments were conducted to answer these questions. We found that, because of the sticky waxy filaments of A. orbigera larvae, A. instabilis is incapable of effectively attacking them and, therefore, the predation rate of A. orbigera on C. viridis does not decrease in the presence of ants. Furthermore, A. instabilis showed aggressive behavior toward A. orbigera's parasitoids, and the presence of ants reduced the parasitism suffered by A. orbigera. This is the first time that this kind of indirect positive effect is reported for an ant and a coccidophagous coccinellid. Furthermore, this indirect positive effect may be key to the persistence of A. orbigera's populations.     

Infiltration of a facultative ant–plant mutualism by the introduced Argentine ant: effects on mutualist diversity and mutualism benefits

1. Ant–plant mutualisms have been the focus of considerable empirical research, but few studies have investigated how introduced ants affect these interactions. Using 2 years of survey data, this study examines how the introduced Argentine ant [Linepithema humile (Mayr)] differs from native ants with respect to its ability to protect the extrafloral nectary‐bearing coast barrel cactus (Ferocactus viridescens) in Southern California. 2. Eighteen native ant species visited cacti in uninvaded areas, but cacti in invaded areas were primarily visited by the Argentine ant. The main herbivore of the coast barrel cactus present at the study sites is a leaf‐footed bug (Narnia wilsoni). 3. Herbivore presence (the fraction of surveys in which leaf‐footed bugs were present on individual cacti) was negatively related to ant presence (the fraction of surveys in which ants were present on individual cacti). Compared with cacti in uninvaded areas, those in invaded areas were less likely to have herbivores and when they did had them less often. 4. Seed mass was negatively related to herbivore presence, and this relationship did not differ for cacti in invaded areas versus those in uninvaded areas. 5. Although the Argentine ant might provide superior protection from herbivores, invasion‐induced reductions in ant mutualist diversity could potentially compromise plant reproduction. The cumulative number of ant species on individual cacti over time was lower in invaded areas and was associated with a shortened seasonal duration of ant protection and reduced seed mass. These results support the hypothesis that multiple partners may enhance mutualism benefits.     

Colourful stripes send mixed messages to safe and risky partners in a diffuse cleaning mutualism

The steps by which neutral, random and/or negative biological interactions evolve into mutualistic ones remain poorly understood. Here, we study Elacatinus gobies and the ‘client’ fishes they clean. Colourful stripes are common to mutualist cleaners and noncleaning sister species. Blue stripes are unique to cleaners and are more conspicuous to predators than are basal yellow or green stripes. In turn, we focused on the role of colour as a potentially specialized signal. We show that cleaners may possess a chemical defence and demonstrate that stripes are sufficient to elicit client posing behaviour and to deter attack, corroborating the putative role of chemistry. Analysis of previously published records shows that yellow cleaners interact with predatory clients less often compared to green and blue cleaners. Our results highlight evolution from predator resistance to advertising with conspicuous signals. Similar trajectories, via recognizable signals to risky partners, may be common in other diffuse mutualisms.     

Costs and benefits of a superinfection of facultative symbionts in aphids

Symbiotic associations between animals and inherited micro-organisms are widespread in nature. In many cases, hosts may be superinfected with multiple inherited symbionts. Acyrthosiphon pisum (the pea aphid) may harbour more than one facultative symbiont (called secondary symbionts) in addition to the obligate primary symbiont, Buchnera aphidicola. Previously we demonstrated that, in a controlled genetic background, A. pisum infected with either Serratia symbiotica or Hamiltonella defensa (called R- and T-type in that study) were more resistant to attack by the parasitoid Aphidius ervi. Here, we examined the consequences of A. pisum superinfected with both resistance-conferring symbionts. We found that an A. pisum line co-infected with both S. symbiotica and H. defensa symbionts exhibits even greater resistance to parasitism by A. ervi than either of the singly infected lines. Despite this added benefit to resistance, superinfections of S. symbiotica and H. defensa symbionts appeared rare in our survey of Utah A. pisum symbionts, which is probably attributable to severe fecundity costs. Quantitative polymerase chain reaction estimates indicate that while the density of H. defensa is similar in singly and superinfected hosts, S. symbiotica densities increased dramatically in superinfected hosts. Over-proliferation of symbionts or antagonistic interactions between symbionts may be harmful to the aphid host. Our results indicate that in addition to host-symbiont interactions, interactions among the symbionts themselves probably play a critical role in determining the distributions of symbionts in natural populations.     

Distance-dependent costs and benefits of aggressive mimicry in a cleaning symbiosis

In aggressive mimicry, a 'predatory' species resembles a model that is harmless or beneficial to a third species, the 'dupe'. We tested critical predictions of Batesian mimicry models, i.e. that benefits of mimicry to mimics and costs of mimicry to models should be experienced only when model and mimic co-occur, in an aggressive mimicry system involving juvenile bluestreaked cleaner wrasse (Labroides dimidiatus) as models and bluestriped fangblennies (Plagiotremus rhinorhynchos) as mimics. Cleanerfish mimics encountered nearly twice as many potential victims and had higher striking rates when in proximity to than when away from the model. Conversely, in the presence of mimics, juvenile cleaner wrasses were visited by fewer clients and spent significantly less time foraging. The benefits to mimic and costs to model thus depend on a close spatial association between model and mimic. Batesian mimicry theory may therefore provide a useful initial framework to understand aggressive mimicry.     

Costs and benefits of defense by tannins in a neotropical tree

Summary The costs and benefits of defense by tannins were investigated for a neotropical tree, Cecropia peltata L. (Moraceae). Seedlings of equal age were grown under uniform conditions in a greenhouse for 18 months. Within a plant, leaf tannin concentrations measured in different years were highly correlated. Tannin concentrations differed substantially among individuals; plants with high tannin content had lower damage levels in herbivory experiments. The effects of tannin on herbivory appeared to be dosage dependent. There was, however, a cost associated with tannin production in terms of reduced leaf production.     

Costs and benefits of induced resistance in a clonal plant network

Plant defense theory suggests that inducible resistance has evolved to reduce the costs of constitutive defense expression. To assess the functional and potentially adaptive value of induced resistance it is necessary to quantify the costs and benefits associated with this plastic response. The ecological and evolutionary viability of induced defenses ultimately depends on the long-term balance between advantageous and disadvantageous consequences of defense induction. Stoloniferous plants can use their inter-ramet connections to share resources and signals and to systemically activate defense expression after local herbivory. This network-specific early-warning system may confer clonal plants with potentially high benefits. However, systemic defense induction can also be costly if local herbivory is not followed by a subsequent attack on connected ramets. We found significant costs and benefits of systemic induced resistance by comparing growth and performance of induced and control plants of the stoloniferous herb Trifolium repens in the presence and absence of herbivores.     

Costs and benefits of genetic heterogeneity within organisms

An increasing number of studies have recently detected within-organism genetic heterogeneity suggesting that genetically homogeneous organisms may be rare. In this review, we examine the potential costs and benefits of such intraorganismal genetic heterogeneity (IGH) on the fitness of the individual. The costs of IGH include cancerous growth, parasitism, competitive interactions and developmental instability, all of which threaten the integrity of the individual while the potential benefits are increased genetic variability, size-specific processes, and synergistic interactions between genetic variants. The particular cost or benefit of IGH in a specific case depends on the organism type and the origin of the IGH. While mosaicism easily arise by genetic changes in an individual, and will be the more common type of IGH, chimerism originates by the fusion of genetically distinct entities, and is expected to be substantially rare in most organisms. Potential conflicts and synergistic effects between different genetic lineages within an individual provide an interesting example for theoretical and empirical studies of multilevel selection.     

Costs and benefits of resistance against antimalarial drugs

Recent experiments have suggested that resistance to antimalarial drugs, in particular chloroquine, is associated with increased transmission. However, epidemiological patterns suggest the opposite: ie. that resistance should be associated with a transmission cost. Here, Jacob Koella reviews the evidence for either a cost or a benefit of chloroquine resistance and proposes ideas from population and evolutionary biology that might explain the apparent contradiction between experimental and epidemiological evidence.