Brighter-colored paper wasps (Polistes dominula) have larger poison glands
© Vidal-Cordero et al.; licensee BioMed Central Ltd. 2012
Received: 20 May 2012
Accepted: 10 July 2012
Published: 20 August 2012
Aposematism is a defense system against predators consisting of the toxicity warning using conspicuous coloration. If the toxin production and aposematic coloration is costly, only individuals in good physical condition could simultaneously produce abundant poison and striking coloration. In such cases, the aposematic coloration not only indicates that the animal is toxic, but also the toxicity level of individuals. The costs associated with the production of aposematic coloration would ensure that individuals honestly indicate their toxicity levels. In the present study, we examine the hypothesis that a positive correlation exists between the brightness of warning coloration and toxicity level using as a model the paper wasp (Polistes dominula).
We collected wasps from 30 different nests and photographed them to measure the brightness of warning coloration in the abdomen. We also measured the volume of the poison gland, as well as the length, and the width of the abdomen. The results show a positive relationship between brightness and poison-gland size, which remained positive even after controlling for the body size and abdomen width.
The results suggest that the coloration pattern of these wasps is a true sign of toxicity level: wasps with brighter colors are more poisonous (they have larger poison glands).
KeywordsPaper wasp Poison glands Aposematic coloration Warning signals
Aposematic coloration is a defense system against predators widely used in the animal kingdom, by which potential prey use their striking coloration to warn a possible predator that they are toxic [1, 2]. Aposematism has learning components, because predators learn to associate aposematic coloration with toxicity after testing the prey . Thus, predators learn to avoid distasteful prey more quickly when the prey is more visible, as opposed to cryptic prey , which, in turn, impels a selective pressure for toxic prey to be as striking as possible, leading to a coevolution between predator and prey .
Becoming and remaining toxic is likely to be costly for individuals, due to costs associated with the production or storage of the toxin . In this case, once predators have learned to avoid aposematic prey coloration, an individual would benefit from having aposematic coloration and decrease the demands of toxicity . This would cause the evolution of warning coloration to be evolutionarily unstable. In this situation, individuals within a population will honestly warn of their toxicity using warning coloration only if the signal is difficult to produce, so that a cheater would not be able to cope with such demands . For example, since the warning coloration is striking, it would attract inexperienced predators, so that an individual with non-toxic aposematic coloration would be attacked with greater probability than an individual with cryptic coloration . In such a case, the cost of attracting predators may be tolerated only by animals which are the brightest and the most toxic in the population . Aposematic color production can also be metabolically costly . Additionally, certain pigment molecules used in the aposematic coloring (e.g., carotenoids, melanin) can act as antioxidants [12, 13]. Consequently, investing in a brighter coloration would be demanding for the animal, making it more susceptible to oxidative stress, because the pigments used in coloration are diverted from combating oxidative stress .
Therefore, if the toxin production and aposematic coloration is demanding, only individuals in good physical condition can simultaneously sustain the production of abundant poison and striking coloration . Therefore aposematic coloration would be a true indicator of the toxicity level in individuals . In fact, birds are able to distinguish subtle differences in the coloration of prey, and they are more cautious with the most colorful individuals . Supporting this idea, ladybirds (Harmonia axyridis and Coccinella septempunctata) show a positive correlation between brightness and toxicity [15, 17]. Although there is evidence of intraspecific variation in levels of aposematic coloration , there are few studies that relate the characteristics of the coloring, such as the brightness, with the poison amount [15, 17].
In the present study we tested the hypothesis that there is a positive correlation between the brightness of the warning coloration and toxicity using the paper wasp (Polistes dominula) as a study model. These wasps, in order to avoid predators, have conspicuous color patterns in yellow and black covering their bodies , and stings armed with the poison gland. The coloration of these wasps depends on environmental conditions  but no study is available on the relationship between the brightness of the coloration and the poison levels. If color is a honest sign of toxicity, wasps with most intense colors (brighter) should be equipped with larger poison glands (and therefore should be able to inject more venom into a potential enemy). To test this prediction, we analyze the relationship between brightness and size of the poison glands in this species.
Multiple-regression model relating poison-gland size with coloration (PCA1 factor), controlling for general body size (PCA2 factor; F 2, 27 = 3.15, p = 0.059, R 2 = 0.19) and for abdomen width (F 2, 27 = 4.61, p = 0.019, R 2 = 0.25)
Controlling for general body size (PCA2)
Controlling for abdomen width
The results of our study show that the size of the poison glands in the paper wasp is positively correlated with the brightness of aposematic coloration of the dorsum of the abdomen. This relationship was not confounded by the size of the insect. Although wasps with wider abdomens showed larger glands, when we controlled for the size of the abdomen, the relationship between the size of the poison gland and the color remained statistically significant. Therefore, the wasps with intense coloration probably have more venom to inject, making them more dangerous for predators. Consequently, our results support the idea that paper wasps indicate their level of toxicity through color, a result similar to that found previously in ladybirds [15, 17]. Individuals with brighter colors, indicating more poison, can be more easily detected by a predator. Therefore, the predator can assess the risk involved in attacking the potential prey and can decide not to attack if the prey is very dangerous [10, 16]. In the case of novice predators, although brighter coloration would seem more attractive, the signal may be associated with more toxic animals, making the defense successful. There is evidence that aposematic prey can survive attacks by inexperienced predators . Moreover, given that these wasps are eusocial, by attacking a very poisonous wasp, the predator may easily learn to avoid the remaining individuals in the colony. Our results therefore support theoretical models that predict that warning coloration can indicate the level of toxicity, not only that the animal is toxic [10, 14].
The positive correlation we found between poison gland size and color suggests that only individuals in good physical condition can cope with the process of developing a significant amount of poison while maintaining an intense color (see ). This would occur if the production of the coloration and the venom compete for a given resource. It can be assumed that both processes require ample energy. Another possibility is that poison production is demanding in terms of oxidative stress, and that the pigments used in aposematic coloring have an antioxidant function . In both cases, individuals would have to reach an optimal level of investment in poison and color according to their body condition, resulting in the observed positive correlation (individuals in better condition being brighter and having larger poison glands). The exact mechanism by which aposematic coloration can indicate the level of toxicity is still unknown, and in fact, we are beginning to discover that color may indicate quantitatively the level of toxicity. An example which shows that aposematic coloration, like other traits, is demanding and requires a trade-off with other aspects of life strategies is shown from the experiments with the wood tiger moth (Parasemia plantaginis), in which there is a polymorphism that remains the same as a result of the balance between survival and mating success. In this species, the white morphotype (not aposematic) has more reproductive success, while the yellow morphotype (aposematic) is more successful in survival against predators .
The results at the intraspecific level (a positive correlation in three studies, see [15, 17]) differ from results at the interspecific level. In frogs of the genus Epipedobates, toxicity negatively correlates with warning coloration , while other studies have correlated brightness and toxicity in frogs from the dendrobatid family  and marine opisthobranchs . At the interpopulation level, no relationship was found between toxicity and coloration between different populations of the frog Dendrobates pumilio in a study , while a positive correlation was found in a more recent study . These conflicting results could be explained by the variation in the costs and benefits of coloration and toxicity according to the ecological characteristics of species or populations . However, while the model of Speed & Ruxton  applies to interpopulation or interspecific variation in aposematic coloration and toxicity, predicting positive or negative correlations according to ecological circumstances, the variation within a population can best be explained by the model of Blount et al.  (also see [10, 28]), which predicts a positive correlation between toxicity and coloration within a given population. This model predicts that warning coloration includes a cost in the signal's production that allows it to be a true indicator of the level of toxicity.
In conclusion, according to the results of our study, paper wasps appear to indicate their toxicity level by the abdomen color (brighter-colored wasps having larger poison glands). These results imply that aposematic coloration may have evolved as a Zahavian signal, and coloration is an accurate indicator of toxicity. Predators, therefore, can use the information provided by the color of their potential prey to decide whether or not to attack, or to measure the level of caution that they must take in an attack.
Polistes dominula has been a good candidate for studies linking the color with other variables, such as the establishment of social status [28–30]. These wasps are eusocial insects, and in southern Spain, the colony-founding process is relatively long (late February to mid-May). The colony process can start with several females, and although all the founders are potentially capable of reproduction, an individual ultimately exerts dominance (alpha queen), laying most of the eggs while the subordinates are responsible for foraging, feeding larvae, and collecting materials for nest building [31–33].
Measuring the color and morphology
Results of the PCA
Red channel (Yellow part)
Green channel (Yellow part)
Blue channel (Yellow part)
Red channel (Black part)
Green channel (Black part)
Blue channel (Black part)
Abdomen length (mm)
Abdomen width (mm)
Head width (mm)
Comments by anonymous referees improved the manuscript. David Nesbitt improved the English.
- Mallet J, Joron M: Evolution of diversity in warning color and mimicry: polymorphisms, shifting balance, and speciation. Annu Rev Ecol Syst. 1999, 30: 201-233. 10.1146/annurev.ecolsys.30.1.201.View Article
- Ruxton GD, Sherratt TN, Speed MP: Avoiding attack: the evolutionary ecology of crypsis, warning signals and mimicry. 2004, Oxford University Press, Oxford UKView Article
- Wiklund C, Jarvi T: Survival of distasteful insects after being attacked by naive birds: a reappraisal of the theory of aposematic coloration evolving through individual selection. Evolution. 1982, 36: 998-1002. 10.2307/2408077.View Article
- Sherratt TN, Beaty CD: The evolution of warning signals as reliable indicators of prey defense. Am Nat. 2003, 162: 377-389. 10.1086/378047.View ArticlePubMed
- Sherratt TN: The coevolution of warning signals. Proc R Soc B. 2002, 269: 741-746. 10.1098/rspb.2001.1944.PubMed CentralView ArticlePubMed
- Holloway GJ, de Jong PW, Brakefield PM, de Vos H: Chemical defence in ladybird beetles (Coccinellidae). I. Distribution of coccinelline and individual variation in defence in 7-spot ladybirds (Coccinella septempunctata). Chemoecology. 1991, 2: 7-14. 10.1007/BF01240660.View Article
- Pfennig DW, Harcombe WR, Pfennig KS: Frequency-dependent Batesian mimicry. Nature. 2001, 410: 323-10.1038/35066628.View ArticlePubMed
- Guilford T, Dawkins MS: Are warning colors handicaps?. Evolution. 1993, 47: 400-416. 10.2307/2410060.View Article
- Zahavi A, Zahavi A: The handicap principle: a missing piece of the Darwin's puzzle. 1997, Oxford University Press, New York
- Speed MP, Ruxton GD, Blount JD, Stephens PA: Diversification of honest signals in a predator-prey system. Ecol Lett. 2010, 13: 744-753. 10.1111/j.1461-0248.2010.01469.x.View ArticlePubMed
- Srygley RB: The aerodynamic costs of warning signals in palatable mimetic butterflies and their distasteful models. Proc R Soc B. 2004, 271: 589-594. 10.1098/rspb.2003.2627.PubMed CentralView ArticlePubMed
- McGraw KJ: The antioxidant function of many animal pigments: are there consistent health benefits of sexually selected colourants?. Anim Behav. 2005, 69: 757-764. 10.1016/j.anbehav.2004.06.022.View Article
- Griffith SC, Parker TH, Olson VA: Melanin-versus carotenoid-based sexual signals: is the difference really so black and red?. Anim Behav. 2006, 71: 749-763. 10.1016/j.anbehav.2005.07.016.View Article
- Blount JD, Speed MP, Ruxton GD, Stephens PA: Warning displays may function as honest signals of toxicity. Proc R Soc B. 2009, 276: 871-877. 10.1098/rspb.2008.1407.PubMed CentralView ArticlePubMed
- Blount JD, Rowland HM, Drijfhout FP, Endler JA, Inger R, Sloggett JJ, Hurst GDD, Hodgson DJ, Speed MP: How the ladybird got its spots: effects of resource limitation on the honesty of aposematic signals. Funct Ecol. 2012, 26: 334-342. 10.1111/j.1365-2435.2012.01961.x.View Article
- Gamberale-Stille G, Tullberg BS: Experienced chicks show biased avoidance of stronger signals: an experiment with natural colour variation in live aposematic prey. Evol Ecol. 1999, 13: 579-589. 10.1023/A:1006741626575.View Article
- Bezzerides AL, McGraw KJ, Parker RS, Husseini J: Elytra color as a signal of chemical defense in the Asian ladybird beetle Harmonia axyridis. Behav Ecol Sociobiol. 2007, 61: 1401-1408. 10.1007/s00265-007-0371-9.View Article
- Stevens M, Ruxton GD: Linking the evolution and form of warning coloration in nature. Proc R Soc B. 2012, 279: 417-426. 10.1098/rspb.2011.1932.PubMed CentralView ArticlePubMed
- Schuler W, Hesse E: On the function of warning coloration: a black and yellow pattern inhibits prey-attack by naive domestic chicks. Behav Ecol Sociobiol. 1985, 16: 249-255. 10.1007/BF00310988.View Article
- Tibbetts EA: The condition dependence and heritability of signaling and nonsignaling color traits in paper wasps. Am Nat. 2010, 175: 495-503. 10.1086/651596.View ArticlePubMed
- Nokelainen O, Hegna RH, Reudler JH, Lindstedt C, Mappes J: Trade-off between warning signal efficacy and mating success in the wood tiger moth. Proc R Soc B. 2012, 279: 257-265. 10.1098/rspb.2011.0880.PubMed CentralView ArticlePubMed
- Darst CR, Cummings ME, Cannatella DC: A mechanism for diversity in warning signals: conspicuousness versus toxicity in poison frogs. Proc Natl Acad Sci USA. 2006, 103: 5852-5857. 10.1073/pnas.0600625103.PubMed CentralView ArticlePubMed
- Summers K, Clough ME: The evolution of coloration and toxicity in the poison frog family (Dendrobatidae). Proc Natl Acad Sci USA. 2001, 98: 6227-6232. 10.1073/pnas.101134898.PubMed CentralView ArticlePubMed
- Cortesti F, Cheney KL: Conspicuousness is correlated with toxicity in marine opisthobranchs. J Evol Biol. 2010, 23: 1509-1518. 10.1111/j.1420-9101.2010.02018.x.View Article
- Daly JW, Myers CW: Toxicity of Panamanian poison frogs (Dendrobates): some biological and chemical aspects. Science. 1967, 156: 970-973. 10.1126/science.156.3777.970.View ArticlePubMed
- Maan ME, Cummings ME: Poison frog colors are honest signals of toxicity, particularly for bird predators. Am Nat. 2012, 179: E1-E14. 10.1086/663197.View ArticlePubMed
- Speed MP, Ruxton GD: How nasty and how bright? Explaining variation in warning displays. Evolution. 2007, 61: 623-635. 10.1111/j.1558-5646.2007.00054.x.View ArticlePubMed
- Lee TJ, Speed MP, Stephens PA: Honest signaling and the uses of prey coloration. Am Nat. 2011, 178: E1-E9. 10.1086/660197.View ArticlePubMed
- Tibbetts EA, Dale J: A socially enforced signal of quality in paper wasp. Nature. 2004, 432: 218-222. 10.1038/nature02949.View ArticlePubMed
- Cervo R, Dapporto L, Beani L, Strassmann JE, Turillazzi S: On status badges and quality signals in the paper wasp Polistes dominulus: body size, facial colour patterns and hierarchical rank. Proc R Soc B. 2008, 275: 1189-1196. 10.1098/rspb.2007.1779.PubMed CentralView ArticlePubMed
- Tibbetts EA, Mettler A, Levy S: Mutual assessment via visual status signals in Polistes dominulus wasps. Biol Lett. 2010, 6: 10-13. 10.1098/rsbl.2009.0420.PubMed CentralView ArticlePubMed
- Theraulaz G, Gervet J, Thon B, Pratte M, Semenoff-Tian-Chanski S: The dynamics of colony organisation in the primitively eusocial wasp Polistes dominulus Christ. Ethology. 1992, 91: 177-202.View Article
- Zanette L, Field J: Cues, concessions, and inheritance: dominance hierarchies in the paper wasp Polistes dominulus. Behav Ecol. 2009, 20: 773-780. 10.1093/beheco/arp060.View Article
- Hurlbert SH: Pseudoreplication and the design of ecological field experiments. Ecol Monogr. 1984, 54: 187-211. 10.2307/1942661.View Article
- Stevens M, Párraga CA, Cuthill IC, Partridge JC, Troscianko TS: Using digital photography to study animal coloration. Biol J Linn Soc. 2007, 90: 211-237. 10.1111/j.1095-8312.2007.00725.x.View Article
- Montgomerie R: Analyzing colors. Bird coloration. Vol. I: Mechanisms and measurements. Edited by: Hill GE, McGraw KJ. 2006, Harvard University Press, Cambridge, 90-147.
- Rasband WS: Image J, version 1.41. 2008, Frederick, Maryland
- Quinn GP, Keough MJ: Experimental design and data analysis for biologists. 2002, Cambridge University Press, CambridgeView Article
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.