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. 2021 Aug 11;17(8):20210316. doi: 10.1098/rsbl.2021.0316

Resource exchange and partner recognition mediate mutualistic interactions between prey and their would-be predators

Luis F Camacho 1,✉, Leticia Avilés 1
PMCID: PMC8355686  PMID: 34376075

Abstract

Animals may develop mutualistic associations with other species, whereby prey offer resources or services in exchange for protection from predators. Alternatively, prey may offer resources or services directly to their would-be predators in exchange for their lives. The latter may be the case of hemipterans that engage in mutualistic interactions with ants by offering a honeydew reward. We test the extent to which a honeydew offering versus partner recognition may play a role as proximate mechanisms deterring ants from predating upon their hemipteran partners. We showed that, when presented with a choice between a hemipteran partner and an alternative prey type, mutualist ants were less likely to attack and more likely to remain probing their hemipteran partners. This occurred even in the absence of an immediate sugary reward, suggesting either an evolved or learned partner recognition response. To a similar extent, however, ants were also less likely to attack the alternative prey type when laced with honey as a proxy for a honeydew reward. This was the case even after the honey had been depleted, suggesting an ability of ants to recognize new potential sources of sugars. Either possibility suggests a degree of innate or learned partner recognition.

Keywords: ant, Hemiptera, Membracidae, mutualism, predation, treehopper

1. Background

Animals exhibit an array of behavioural strategies that reduce their risk of being predated upon [1–3]. In addition to simple strategies, such as escaping or hiding, animals may have evolved more complex behaviours such as forging mutualistic interactions, whereby prey may offer resources or services to other species in exchange for protection from predators [4–6]. Alternatively, prey may offer resources or services directly to the predators themselves to avoid becoming their meal [7,8]. This creates the interesting case of mutualistic interactions being mediated by a predator's reluctance to attack.

Ants engaging in mutualistic interactions with sap-sucking hemipterans (e.g. Aphididae, Coccidae, Aetalionidae and Membracidae) are a prime example of a predator–prey mutualistic interaction. Ants are widely recognized to provide a variety of services to hemipterans, most notably protection from predators [7,9]. Ants, however, are themselves major predators of arthropods and may also predate on their hemipteran partners [10–14]. Hemipterans are known to appease ants with honeydew, which, despite being a waste product, is typically enriched with carbohydrates and amino acids relinquished from sap [15–21]. It has been shown that ants that complement a protein-rich diet with honeydew have greater colony growth and reduced worker and brood mortality [22,23].

The nutritional value derived from honeydew may, thus, be the primary proximate mechanism appeasing the ants. In this case, ant appeasement would depend on a constant supply of honeydew regardless of identity of the producer. Alternatively, ants may refrain from predating on their hemipteran partners, even in the absence of a honeydew offering, if they recognize their partners through partner recognition mechanisms. Whether appeasement depends on a honeydew offering, partner recognition, or both may reflect the extent to which the predatory aspect of the interaction is mediated by a direct stimulus (honeydew only) or by innate partner recognition.

To determine the relative roles of honeydew and partner recognition as proximate mechanisms deterring ants from predating upon their hemipteran partners, we performed choice experiments with sap-sucking hemipterans and an alternative prey type, in the presence or absence of honey as a proxy for a honeydew reward. The ants refraining from predating on hemipteran baits in the absence of honeydew would suggest partner recognition through either learned or evolved responses. Ants refraining from predating on non-hemipteran baits laced with honey, on the other hand, would be indicative of a protective effect of honeydew above and beyond partner recognition. Apart from appeasing the ants, honey or partner recognition may elicit the ants' attention, where ants may remain probing the baits rather than abandon them. If ants were more likely to probe their hemipteran partner than non-partner baits, this would provide further support for the partner recognition hypothesis. Likewise, were ants more likely to probe baits with honey than without, this would support the honeydew appeasing hypothesis.

2. Methods

We carried out our choice experiments during June and July of 2018 at the Jatun Sacha Biological Reserve (1°3'58.33″ S; 77°36'59.69″ W) in the Amazonian rainforest in eastern Ecuador, where ant–hemipteran mutualistic interactions are ubiquitous. We chose adult treehoppers (Hemiptera: Membracidae and Aetalionidae; electronic supplementary material, table S1) as the ant-mutualist baits, as treehoppers are frequent ant associates [7,24]. We used termite workers (Nasutitermes) as the alternative, non-mutualist bait, as they are of comparable size and armour to treehoppers, but have a different chemical identity. In both cases, baits were locally collected. As treehopper baits reflected local communities in both composition and relative abundance, we carried out a separate analysis focusing exclusively on treehopper baits to assess ant predation on treehoppers with different degrees of mutualism, which we classified based on the natural history of the respective genera (electronic supplementary material, table S1) [24]. In comparisons with termite baits, we excluded from the analyses the 5% treehopper baits that belonged to non-mutualist treehopper genera. In addition to the treehoppers, we also collected and classified the ants that interacted with the baits according to their mutualistic tendencies, also based on the natural history of their genera (electronic supplementary material, table S2) [25]. We identified ant specimens based on Bolton [26] and updated taxonomic names based on AntCat [27]. Voucher specimens were deposited in the QCAZ Invertebrate Museum at the Pontificia Universidad Católica del Ecuador. Electronic supplementary material, tables S1 and S2 provide details of the classification of treehopper baits, and of the ants that interacted with them, as mutualists (53% treehoppers, 91% ants), partial mutualists (42% treehoppers, 7% ants) or non-mutualists (5% treehoppers, 2% ants).

Both treehopper and termite baits were newly immobilized by freezing to maintain the integrity of their cuticular chemistry, which is likely to play a role in the ants’ decision to attack or refrain from attacking [28–30]. We were also careful not to contaminate the baits with sweat as this could influence the ants' behaviour towards the baits [31]. We placed the baits in treatment combinations involving either the same or a different prey type, with and without honey. The vast majority of treehopper couplets consisted of specimens of the same genus, with only five exceptions (3.8%) resulting from constraints of local treehopper availability. We added an approximately 1 mm diameter droplet of honeybee honey on the tip of the prey's abdomen, which roughly approximates a honeydew offering, as both contain protein, in addition to sugars [32]. Although the sugar composition of honey (mostly disaccharides) differs from that of honeydew (mostly trisaccharides), ants are known to accept a variety of sugar types [33,34].

In the experiment, we established 12 transects consisting of six replicates of two transect types: transects with couplets of the same specimen type (treehopper or termite), one with honey, the other without; or couplets of different specimen types, both with or both without honey. This setup allowed us to separate the effects of specimen type versus those of presence or absence of honey. Couplets in each transect were set up on vegetation overhanging from the canopy, with the alternative bait types attached with PVA glue to opposing stems of a bifurcation (electronic supplementary material, figure S1A). With couplets separated by at least 5 m from one another, each transect contained 10 couplets of each of the alternative bait types, deployed in alternating arrangement, for a total of 20 couplets per transect. Transects of the two types were placed in comparable locations on the landscape, separated by at least 100 m and surveyed on rainless days between 9.00 and 14.00, alternating transect types across days to minimize possible effects of weather. We monitored the baits at 30 min intervals for 3 h and recorded whether ants were attacking, probing or absent. Attacks were recorded when ants were actively biting the baits, dismembering them, or carrying them away. Probing was recorded when ants remained with the baits, touching them with their antennae and legs but not biting. We also monitored whether ants consumed the honey droplet, which always took place between 30 and 60 min after the baits had been discovered.

We used a Cox proportional hazards mixed-effects model (CMM), which controls for the time dependence of predation events while testing the effects of each fixed factor simultaneously and independently, to assess ant predation on treehoppers with different degrees of mutualism. Considering only treehopper baits, the model included transect type, presence or absence of honey, and treehopper mutualism type (mutualist, partial mutualist, non-mutualist) as fixed factors. Treehopper genus, ant genus and bait couplet nested within transect served as random effects (table 1, model C). In this model, we only included ant genera that had interacted with all treehopper mutualism types (Camponotus, Crematogaster, Dolichoderus, Ectatomma; electronic supplementary material, table S2 and figure S2).

Table 1.

Models used to test for the probability of predation by ants in relation to bait type (treehoppers or termites, model A; or treehoppers with different degrees of association with ants, model C) and the presence or the absence of added honey. Models A and C test for predation rate over time using Cox proportional hazards mixed-effects models (CMM). Model B uses generalized linear mixed-effects models (GLMM) to test for the probability of ants continuing to probe the baits (treehopper or termite) rather than abandon them following discovery. Models' coefficients are relative to termites, in specimen type; baits without honey, on honey treatment; transects with honey couplets, in transect type; and non-mutualist treehoppers in treehopper type. Values of p below 0.05 are shown in italics.

model/response variable fixed factor odds ratio log odds ± est. error χ2 p
model A (CMM):
 proportional predation risk specimen type: 80.38 <0.01
 treehopper 0.32 −1.14 ± 0.13  
honey treatment: 73.47 <0.01
 honey on baits 0.34 −1.06 ± 0.12
transect type: 0.26 0.61
 specimen couplets 1.11 0.09 ± 0.19
model B (GLMM):
 probability of probing rather than abandoning specimen type: 1.19 0.27
 treehopper 1.65 0.50 ± 0.46
honey treatment: 11.11 <0.01
 honey on baits 4.44 1.49 ± 0.44
transect type: 0.02 0.88
 specimen couplets 0.93 −0.07 ± 0.50
minutes after discovery 0.96 −0.04 ± 0.003 105.38 <0.01
model C (CMM):
 proportional predation risk treehopper type: 7.48 0.02
 mutualist 0.58 −0.55 ± 0.45
 partial mutualist 0.29 −1.22 ± 0.48
honey treatment: 34.34 <0.01
 honey on baits 0.22 −1.49 ± 0.25
transect type: 2.2 0.14
 specimen couplets 2.25 0.81 ± 0.55
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We used another CMM to test for differences between treehopper and termite treatments. We included experiment type, the presence or the absence of honey and specimen type as fixed factors (table 1, model A), and bait couplet (n = 120 per transect type) nested within transect (n = 6 of each transect type) as random effect. We excluded baits with non-mutualist treehoppers (5%).

In both CMM, we also excluded baits predated by unknown predators (likely non-ant) (2.31% of all baits). Baits not registering an attack within the 3 h monitoring period were coded as right-censored (10% of all baits).

We used a general linear mixed-effects model (GLMM) with a logit function and binomial error distribution to test whether at each 30 min time interval baits encountered by ants, but not predated upon, were being probed or were abandoned by the ants. Whether baits were being probed (coded as 1) or had been abandoned (coded as 0) served as the response variable. Transect type, time interval, bait type and the presence or the absence of honey served as fixed factors, with individual baits (n = 240 per transect type), nested within bait couplet (n = 120 per transect type), nested within transect (n = 6 per type), as random effects (table 1, model B).

All statistical analyses were carried out in R v. 3.2.2 software [35]. We used packages dplyr for data manipulation [36], survival [37] for construction of Cox models and coxme [38] to incorporate random effects, glmmTMB [39] for GLMM construction and car [40] for p-value calculations, ggplot2 [41], ggpubr [42] and lemon [43] for figure design. Data and R code are available in Dryad [44].

3. Results

Following discovery, ants were 68% less likely (1–0.32 odds ratio in table 1 model A) to predate upon treehoppers compared with termite baits and 66% less likely to predate on baits with honey than on baits without honey (figure 1a; table 1, model A; figure S1B). Ants' propensity to predate upon baits was independent of the type of couplets they encountered as there were no significant differences in predation rate on baits of a particular type across the two choice-type experiments (table 1, model A). After ants depleted the honey from treehopper and termite baits, predation rate did not increase to match that of baits without honey (figure S1C).

Figure 1.

Figure 1.

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(a) Proportion of baits over time predated by ants following discovery. (b) Among surviving baits, proportion being probed rather than abandoned (termite line disappears after 60 min because all baits had been predated at that point). Lines represent means from all 12 transects, each with 20 couplets of various types.

When considering the behaviour of ants that did not predate on baits (figure 1b), we found that ants were 4.4 times more likely to remain probing rather than abandon baits, either treehopper or termite, that originally had honey compared with those without (table 1, model B). In terms of probing or abandoning baits, ants showed no difference in their behaviour towards treehopper or termite baits (figure 1b and table 1, model B).

When focusing on treehopper baits, partially mutualist and mutualist treehopper genera were, respectively, 70 and 42% less likely to be attacked by ants compared with non-mutualist genera (figure 2; table 1, model C; and electronic supplementary material, figure S2). Reduced ant aggression to these types of treehoppers appeared to be stronger when baits were laced with honey, albeit we lacked the degrees of freedom to statistically test this interaction (figure 2). After ants depleted the honey from baits, predation rate on non-mutualist treehoppers, but not on partially mutualist or mutualist treehoppers, increased to match that of baits without honey (figure 2).

Figure 2.

Figure 2.

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Proportion of predated baits following discovery, for treehoppers with various degrees of association with mutualist ants. Lines correspond to mean predation per treehopper/ant genus combination, averaged per treehopper mutualism type, then averaged across transects. For details of interactions between genera, see electronic supplementary material, figure S2.

4. Discussion

We found that the presence either of honey or of an ant-mutualist species, when compared with control baits consisting of non-mutualists with no honey, reduced the likelihood of predation by ants to a similar extent (figures 1a and 2). Moreover, even after the honey was depleted, ants did not increase their propensity to predate upon mutualist treehopper and termite baits that had originally contained honey (figure 1a). Instead, ants tended to continue probing these baits rather than attack or abandon them (figure 1b). Our choice experiments thus provided evidence of a protective effect of honeydew, as well as apparent partner recognition on the part of the ants.

The appeasing effect of honeydew has been demonstrated under experimental conditions involving a few species of ants and several species of aphids (Hemiptera, Aphididae) [45–47]. We showed that this effect also occurs in natural communities of ants interacting with a variety of treehopper species, including two families (Aetalionidae and Membracidae) and four of the seven membracid subfamilies occurring in neotropical rainforests (electronic supplementary material, tables S1 and S2). The ants’ preference for honey, rather than the protein in our prey baits, suggests that satisfying the carbohydrate demands of their colonies is an important ecological driver of the ants' mutualistic association with hemipterans in this habitat [48,49].

In terms of partner recognition, given the opportunistic predatory nature of ants, it is not surprising that they fed readily on termites. What is intriguing is that they avoided feeding on mutualist treehoppers even when these lacked a sugary reward. This suggests some level of recognition of the treehopper partners above and beyond their association with honeydew [29,30,45,46,50]. Here, hemipteran cuticular hydrocarbons may play a role by providing chemical crypsis and/or partner signalling, as shown in reports of treehoppers mimicking the chemical composition of their host plants [51], or aphids mimicking their ant partner's chemical signalling [28]. Possible partner recognition through cuticular hydrocarbons or other means is suggestive of a co-evolved behavioural adaptation between the mutualistic partners, through either an innate or a learned response based on past interactions [28,30,45,50,52,53]. The reduced aggression of ants towards termites laced with honey, even after honey had been depleted, further suggests that ants may also learn to recognize novel sources of sugar [28].

Sap-sucking Hemiptera preceded ants by at least 150 Myr and were producing honeydew to excrete excess sugar in their diet long before ants could exert any predation [7,54,55]. The direct stimulus of honeydew offerings likely played a role in appeasing early ants, which are thought to have been mainly predatory organisms [55,56]. With time, ants may have evolved to recognize the potential for sugar in their hemipteran prey and provide them a range of ecological services such as protection from other predators. In turn, this would have prompted hemipterans to evolve gregarious behaviors and the ability to increase nutrient concentration in honeydew, both important mechanisms facilitating ant appeasement and provision of services today [57–59]. As ants then became the dominant predators across tropical canopies approximately 50 Ma [49,55,56], their success may have been facilitated by their newly acquired ability to exploit hemipteran honeydew [49,55,56].

5. Conclusion

We show that both a sugary reward and partner recognition reduce the risk of predation by ants to a comparable extent, suggesting a role of these mechanisms in enticing ants to associate with hemipterans, rather than prey upon them. The ants' ability—innate or learned—to recognize hemipteran partners suggests a common evolutionary history mediating the ant–hemipteran mutualism. Likewise, the reduced rate of predation on alternative bait types laced with honey points to an ability on the part of the ants to recognize potentially novel sources of sugar. Studying the behaviour of mutualist ants towards hemipteran taxa with various degrees of interdependence could further clarify the role of partner recognition and appeasement as mechanisms mediating mutualistic associations between prey and their would-be predators [50].

Acknowledgements

We thank Ana Ávila for assistance in the field and the QCAZ Invertebrate Museum at the Pontificia Universidad Católica del Ecuador, for their support.

Ethics

The research was conducted under permit no. 003-17-IC-FAU-DNB/MA of the Ecuadorian Ministry of Environment.

Data accessibility

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.pg4f4qrq2 [44].

Authors' contributions

L.C. and L.A. designed the experiment, and wrote and edited the manuscript. L.C. collected and analysed the data. Both authors approved the final version of the manuscript to be published and agree to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved.

Competing interests

We declare we have no competing interests.

Funding

The study was funded by the Programa de Becas de Excelencia SENESCYT of the Ecuadorian government to L.C. and NSERC Discovery and Accelerator awards to L.A.

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Associated Data

This section collects any data citations, data availability statements, or supplementary materials included in this article.

Data Citations

  1. Camacho L. 2021. Data from: Ant predation towards termite and treehopper baits in the Ecuadorian Amazon. Dryad Digital Repository. ( 10.5061/dryad.pg4f4qrq2) [DOI]

Data Availability Statement

Data available from the Dryad Digital Repository: https://doi.org/10.5061/dryad.pg4f4qrq2 [44].

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