- Email: [email protected]
Botanical parasitism of an insect by a parasitic plant
Current Biology
Magazine
FURTHER READING Bertamini, M., Makin, A., and Rampone, G. (2013). Implicit association of symmetry with positive valence, high arousal and simplicity. i-Perception 4, 317–327. Chatterjee, A., and Vartanian, O. (2014). Neuroaesthetics. Trends Cogn. Sci. 18, 370–375. Graf, L.K.M., and Landwehr, J.R. (2015). A dualprocess perspective on fluency-based aesthetics: the pleasure-interest model of aesthetic liking. Pers. Soc. Psychol. Rev. 19, 395–410. Ishizu, T., and Zeki, S. (2011). Toward a brain-based theory of beauty. PLoS One 6, e21852. Jacobsen, T., and Beudt, S. (2017). Stability and variability in aesthetic experience: a review. Front. Psychol. 8, 1–14. Leder, H., and Nadal, M. (2014). Ten years of a model of aesthetic appreciation and aesthetic judgments: the aesthetic episode — developments and challenges in empirical aesthetics. Br. J. Psychol. 105, 443–446. Ma, D.S., Correll, J., and Wittenbrink, B. (2015). The Chicago face database: A free stimulus set of faces and norming data. Behav. Res. Methods 47, 1122–1135. Nadal, M., and Pearce, M.T. (2011). The Copenhagen Neuroaesthetics conference: prospects and pitfalls for an emerging field. Brain Cogn. 76, 172–183. Palmer, S.E., Schloss, K.B., and Sammartino, J. (2013). Visual aesthetics and human preference. Annu. Rev. Psychol. 64, 77–107. Pearce, M.T., Zaidel, D.W.W., Vartanian, O., Skov, M., Leder, H., Chatterjee, A., and Nadal, M. (2016). Neuroaesthetics: the cognitive neuroscience of aesthetic experience. Perspect. Psychol. Sci. 11, 265–279. Pelowski, M., Markey, P.S., Lauring, J.O., and Leder, H. (2016). Visualizing the impact of art: an update and comparison of current osychological models of art experience. Front. Hum. Neurosci. 10, 1–21. Redies, C. (2015). Combining universal beauty and cultural context in a unifying model of visual aesthetic experience. Front. Hum. Neurosci. 9, 1–20. Watson, A.B. (1986). Temporal sensitivity. In Handbook of Perception and Human Performance, eds. Boff. K.R., Kaufman, L., and Thomas, J.P. (Wiley: New York), pp. 6/1–6/43. 1 New York University, Department of Psychology, 6 Washington Place, New York, NY 10003, USA. 2Department of Psychology and Center for Neural Science, 4 Washington Place, New York, NY 10003, USA. E-mail: [email protected] (A.A.B.), [email protected] (D.G.P.)
Correspondence
Botanical parasitism of an insect by a parasitic plant Scott P. Egan*, Linyi Zhang, Mattheau Comerford, and Glen R. Hood We report evidence of a new trophic interaction in nature whereby a parasitic plant attacks multiple species of insects that manipulate plant tissue when the two co-occur on a shared primary host plant. Most plant species are attacked by a great diversity of external and internal herbivores [1]. One common herbivore guild, gall-forming insects, induce tumor-like structures of nutrient-rich plant tissue within which immature insects feed and develop [2,3]. While the gall is made of plant A
tissue, its growth and development are controlled by the insect and it therefore represents an extended phenotype of the gall former [4]. Typically, parasitic plants attack other plants to gain nutritional requirements by connecting directly to the vascular system of their hosts using modified root structures called haustoria [5]. Here, we document the first observation of a parasitic plant attacking the insect-induced galls of multiple gall-forming species and provide evidence that this interaction negatively affects gall former fitness. In a native scrub habitat in southern Florida, USA (27°1’ 39.9648’’ N; 80°6’ 33.444’’ W), we discovered the parasitic love vine, Cassytha filiformis (Lauraceae), attacking two species of gall-forming cynipid wasps on the sand live oak, Quercus geminata (Fagaceae). The gall wasp most commonly parasitized by C. filiformis was Belonocnema treatae (Hymenoptera: Cynipidae), which forms spherical,
B
Cassytha vine Haustoria B. treatae leaf gall C 8
D Mummified adult inside gall?
Gall size (mm)
insight into several aspects of aesthetic experience. Stimulus-focused studies have determined key object properties that, on average, increase or decrease the aesthetic appeal of an object, such as symmetry and curvature. Responsefocused studies have started to describe the processes that underlie aesthetic pleasure and their neural correlates independent of stimulus properties. So far, research indicates that aesthetic response requires successful early sensory processing and that there is an especially tight, linear relation between beauty and pleasure responses. Neurally, parts of the ventro-medial orbitofrontal cortex play a crucial role for processing beauty across many stimulus modalities.
6
% 2%
- yes
- no
4 45% 2 0
Unparasitized gall
Gall parasitized by C. filiformis
Unparasitized gall
Gall parasitized by C. filiformis
Figure 1. A trophic inversion involving a parasitic plant and a gall former. (A) Cassytha filiformis vine attaching haustoria to a leaf gall induced by the wasp Belonocnema treatae on the underside of their host plant, Quercus geminata. (B) Labeled graphic of insect gall, parasitic vine, and vine haustoria. (C) Box plots of leaf gall diameter for unparasitized galls (control) and galls that have been parasitized by C. filiformis. (D) Proportion of B. treatae leaf galls that contained a dead ‘mummified’ adult for unparasitized galls (control) and galls that have been parasitized by the vine C. filiformis.
Current Biology 28, R847–R870, August 20, 2018 © 2018 Elsevier Ltd. R863
Current Biology
Magazine single-chambered galls on the underside of new leaves (Figure 1A,B). From a field survey of 2,000 B. treatae galls, we observed 58 (2.9%) attacked by the parasitic vine. Additionally, we measured the location where haustoria typically attach to the host plant (N=718 observations). Interestingly, C. filiformis form haustoria on new stems (40%), buds (10%), petioles (9.5%), and on the top (27%) and edge (12%) of leaves. (Note: the remaining 1.5% of haustoria connections are back onto C. filiformis vines.) However, we never observed haustoria connected to the underside of leaves where B. treatae exclusively induce galls (see Supplemental Information, published with this article online, for details), suggesting that gall attacks by C. filiformis are not due to chance encounters. The number of haustoria directly penetrating B. treatae galls ranged from one to four (mean=1.24±0.08 SE). A cross-section of the haustoria–gall connection reveals that the outer wall of the gall is broken, and the gall wall and inner gall tissue are both ‘turned up’ into the haustoria where nutrients and moisture can be extracted by the vine (Figure S1A,B). The presence of C. filiformis haustoria connected to B. treatae galls was associated with differences in gall size, an important phenotype that influences natural enemy attack and serves as a proxy for wasp fitness [6,7]. Of 152 galls measured, those galls with haustoria attached were 35% larger (n=51; mean diameter=5.57 ± 0.14 mm SE) than galls not parasitized (n=101; 4.11±0.19 mm SE; t=5.01; P<0.0001; Figure 1C). This difference was driven by the lack of smaller galls attacked by C. filiformis (Supplemental Information: K-S test: D=0.4754; P<0.0001; Figure S1C), where no gall smaller than 3.50 mm in diameter was parasitized. Although larger, attacked galls were associated with a negative effect on gall wasp survival. We dissected 51 B. treatae galls attacked by C. filiformis and 23 had a dead ‘mummified’ adult B. treatae inside (45%). For the 101 B. treatae galls not attacked by C. filiformis, we found only 2 individuals with dead adult B. treatae (2%; all other galls possessed an emergence hole made by either the gall wasp or natural enemy). The difference in the proportion of dead wasps associated with C. filiformis attack was highly significant R864
among all galls (2=45.85, P<0.0001; Figure 1D), even after limiting our comparison to galls of a similar size (by dropping all galls below 3.5 mm in diameter; 2=28.02, P<0.0001), suggesting that C. filiformis has an important negative impact on gall wasp survival. Consistent with this being a potentially general, but previously unrecognized, trophic interaction, C. filiformis haustoria were observed directly attacking a large multichambered stem swelling gall induced by a second, but less abundant, gall-forming wasp, Callirhytis quercusbatatoides, at the same site in southern Florida (Figure S2A,B). Of the 65 galls surveyed, attack of C. quercusbatatoides was observed 11 times (17%), with a range of one to five haustoria connected to a single gall (mean=1.50±0.44 SE). Once again, C. filiformis parasitism was associated with a modified gall phenotype. Here, C. quercusbatatoides galls attacked by the vine were 13.5% smaller (n=11; mean diameter for parasitized galls ± SE=14.41±0.64 mm) than non-parasitized galls (n=54; mean diameter for galls not parasitized ± SE=16.65±0.47 mm; t=2.07; P=0.043). In addition, C. filiformis was found in association with five other gall-forming species, including two wasps that induce galls on the bottom of new leaves (Andricus quercuslanigera, Neuroterus minutissimus), where C. filiformis were also found to form haustoria. In addition, C. filiformis was found in association with five other gall-forming species. This included two wasps that induce galls on the bottom of new leaves (Andricus quercuslanigera, Neuroterus minutissimus), where the vine was also found to form haustoria, and two wasps (Disholcaspis quercusvirens, A. quercusfoliatus) and one gall forming fly (Arnoldiola atra [Cecidomyidae: Diptera]) that manipulate stems or buds, where the vine was observed to wrap tightly, multiple times, directly below the gall and initiate haustoria into the stem tissue (Figure S2C). Is this truly a new trophic interaction? Certainly, it is well documented that carnivorous plants can consume insects directly [8], and there is evidence that parasitic plants can indirectly alter host plant interactions
Current Biology 28, R847–R870, August 20, 2018
with other herbivorous community members [9,10]. There is also evidence that other guilds of parasitic wasps (such as inquilines) can attack and manipulate the gall formation process, sometimes killing the gall former [3]. However, this is the first report of a parasitic plant directly attacking an insect-induced plant structure that negatively impacts the insects’ fitness and/or survival. How common is this new trophic interaction in nature? The potential is global in scale, as parasitic plants comprise 1% of angiosperm diversity (~4,500 species in 20 families) [5] and gall formation has been described in over 13,000 species in six insect orders [2,3], and both live in almost every terrestrial habitat on Earth. SUPPLEMENTAL INFORMATION Supplemental Information contains two figures and experimental procedures, and can be found with this article online at https://doi. org/10.1016/j.cub.2018.06.024. REFERENCES 1. Futuyma, D.J., and Agrawal, A.A. (2009). Macroevolution and the biological diversity of plants and herbivores. Proc. Natl. Acad. Sci. USA 106, 18054–18061. 2. Stone, G.N., and Schönrogge, K. (2003). The adaptive significance of insect gall morphology. Trends Ecol. Evol. 18, 512–522. 3. Stone, G.N., Schönrogge, K., Atkinson, R.J., Bellido, D., and Pujade-Villar, J. (2002). The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annu. Rev. Entomol. 47, 633–668. 4. Dawkins, R. (1982). The Extended Phenotype: The Long Reach of the Gene (New York: Oxford). 5. Westwood, J.H., Yoder, J.I., Timko, M.P., and Depamphilis, C.W. (2010). The evolution of parasitism in plants. Trends Plant Sci. 15, 227–235. 6. Egan, S.P., and Ott, J.R. (2007). Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. Ecology 88, 2869–2879. 7. Egan, S.P., Hood, G.R., and Ott, J.R. (2011). Variable selection on gall size: differential contributions of individual host plants to population wide patterns. Evolution 65, 3543–3557. 8. Cameron, K.M., Wurdack, K.J., and Jobson, R.W. (2002). Molecular evidence for the common origin of snap-traps among carnivorous plants. Am. J. Bot. 89, 1503–1509. 9. Press, M.C., and Phoenix, G. K. (2005). Impacts of parasitic plants on natural communities. New Phytol. 166, 737–751. 10. Manrique, V., Cuda, J.P., Overhold, W.A., and Ewe, S.M.L. (2009). Synergistic effect of insect herbivory and plant parasitism on the performance of the invasive tree Schinus terebinthifolius. Entomol. Exp. Appl. 132, 118–125.
Department of BioSciences, Rice University, Houston, TX 77005, USA. *E-mail: [email protected]
Magazine
FURTHER READING Bertamini, M., Makin, A., and Rampone, G. (2013). Implicit association of symmetry with positive valence, high arousal and simplicity. i-Perception 4, 317–327. Chatterjee, A., and Vartanian, O. (2014). Neuroaesthetics. Trends Cogn. Sci. 18, 370–375. Graf, L.K.M., and Landwehr, J.R. (2015). A dualprocess perspective on fluency-based aesthetics: the pleasure-interest model of aesthetic liking. Pers. Soc. Psychol. Rev. 19, 395–410. Ishizu, T., and Zeki, S. (2011). Toward a brain-based theory of beauty. PLoS One 6, e21852. Jacobsen, T., and Beudt, S. (2017). Stability and variability in aesthetic experience: a review. Front. Psychol. 8, 1–14. Leder, H., and Nadal, M. (2014). Ten years of a model of aesthetic appreciation and aesthetic judgments: the aesthetic episode — developments and challenges in empirical aesthetics. Br. J. Psychol. 105, 443–446. Ma, D.S., Correll, J., and Wittenbrink, B. (2015). The Chicago face database: A free stimulus set of faces and norming data. Behav. Res. Methods 47, 1122–1135. Nadal, M., and Pearce, M.T. (2011). The Copenhagen Neuroaesthetics conference: prospects and pitfalls for an emerging field. Brain Cogn. 76, 172–183. Palmer, S.E., Schloss, K.B., and Sammartino, J. (2013). Visual aesthetics and human preference. Annu. Rev. Psychol. 64, 77–107. Pearce, M.T., Zaidel, D.W.W., Vartanian, O., Skov, M., Leder, H., Chatterjee, A., and Nadal, M. (2016). Neuroaesthetics: the cognitive neuroscience of aesthetic experience. Perspect. Psychol. Sci. 11, 265–279. Pelowski, M., Markey, P.S., Lauring, J.O., and Leder, H. (2016). Visualizing the impact of art: an update and comparison of current osychological models of art experience. Front. Hum. Neurosci. 10, 1–21. Redies, C. (2015). Combining universal beauty and cultural context in a unifying model of visual aesthetic experience. Front. Hum. Neurosci. 9, 1–20. Watson, A.B. (1986). Temporal sensitivity. In Handbook of Perception and Human Performance, eds. Boff. K.R., Kaufman, L., and Thomas, J.P. (Wiley: New York), pp. 6/1–6/43. 1 New York University, Department of Psychology, 6 Washington Place, New York, NY 10003, USA. 2Department of Psychology and Center for Neural Science, 4 Washington Place, New York, NY 10003, USA. E-mail: [email protected] (A.A.B.), [email protected] (D.G.P.)
Correspondence
Botanical parasitism of an insect by a parasitic plant Scott P. Egan*, Linyi Zhang, Mattheau Comerford, and Glen R. Hood We report evidence of a new trophic interaction in nature whereby a parasitic plant attacks multiple species of insects that manipulate plant tissue when the two co-occur on a shared primary host plant. Most plant species are attacked by a great diversity of external and internal herbivores [1]. One common herbivore guild, gall-forming insects, induce tumor-like structures of nutrient-rich plant tissue within which immature insects feed and develop [2,3]. While the gall is made of plant A
tissue, its growth and development are controlled by the insect and it therefore represents an extended phenotype of the gall former [4]. Typically, parasitic plants attack other plants to gain nutritional requirements by connecting directly to the vascular system of their hosts using modified root structures called haustoria [5]. Here, we document the first observation of a parasitic plant attacking the insect-induced galls of multiple gall-forming species and provide evidence that this interaction negatively affects gall former fitness. In a native scrub habitat in southern Florida, USA (27°1’ 39.9648’’ N; 80°6’ 33.444’’ W), we discovered the parasitic love vine, Cassytha filiformis (Lauraceae), attacking two species of gall-forming cynipid wasps on the sand live oak, Quercus geminata (Fagaceae). The gall wasp most commonly parasitized by C. filiformis was Belonocnema treatae (Hymenoptera: Cynipidae), which forms spherical,
B
Cassytha vine Haustoria B. treatae leaf gall C 8
D Mummified adult inside gall?
Gall size (mm)
insight into several aspects of aesthetic experience. Stimulus-focused studies have determined key object properties that, on average, increase or decrease the aesthetic appeal of an object, such as symmetry and curvature. Responsefocused studies have started to describe the processes that underlie aesthetic pleasure and their neural correlates independent of stimulus properties. So far, research indicates that aesthetic response requires successful early sensory processing and that there is an especially tight, linear relation between beauty and pleasure responses. Neurally, parts of the ventro-medial orbitofrontal cortex play a crucial role for processing beauty across many stimulus modalities.
6
% 2%
- yes
- no
4 45% 2 0
Unparasitized gall
Gall parasitized by C. filiformis
Unparasitized gall
Gall parasitized by C. filiformis
Figure 1. A trophic inversion involving a parasitic plant and a gall former. (A) Cassytha filiformis vine attaching haustoria to a leaf gall induced by the wasp Belonocnema treatae on the underside of their host plant, Quercus geminata. (B) Labeled graphic of insect gall, parasitic vine, and vine haustoria. (C) Box plots of leaf gall diameter for unparasitized galls (control) and galls that have been parasitized by C. filiformis. (D) Proportion of B. treatae leaf galls that contained a dead ‘mummified’ adult for unparasitized galls (control) and galls that have been parasitized by the vine C. filiformis.
Current Biology 28, R847–R870, August 20, 2018 © 2018 Elsevier Ltd. R863
Current Biology
Magazine single-chambered galls on the underside of new leaves (Figure 1A,B). From a field survey of 2,000 B. treatae galls, we observed 58 (2.9%) attacked by the parasitic vine. Additionally, we measured the location where haustoria typically attach to the host plant (N=718 observations). Interestingly, C. filiformis form haustoria on new stems (40%), buds (10%), petioles (9.5%), and on the top (27%) and edge (12%) of leaves. (Note: the remaining 1.5% of haustoria connections are back onto C. filiformis vines.) However, we never observed haustoria connected to the underside of leaves where B. treatae exclusively induce galls (see Supplemental Information, published with this article online, for details), suggesting that gall attacks by C. filiformis are not due to chance encounters. The number of haustoria directly penetrating B. treatae galls ranged from one to four (mean=1.24±0.08 SE). A cross-section of the haustoria–gall connection reveals that the outer wall of the gall is broken, and the gall wall and inner gall tissue are both ‘turned up’ into the haustoria where nutrients and moisture can be extracted by the vine (Figure S1A,B). The presence of C. filiformis haustoria connected to B. treatae galls was associated with differences in gall size, an important phenotype that influences natural enemy attack and serves as a proxy for wasp fitness [6,7]. Of 152 galls measured, those galls with haustoria attached were 35% larger (n=51; mean diameter=5.57 ± 0.14 mm SE) than galls not parasitized (n=101; 4.11±0.19 mm SE; t=5.01; P<0.0001; Figure 1C). This difference was driven by the lack of smaller galls attacked by C. filiformis (Supplemental Information: K-S test: D=0.4754; P<0.0001; Figure S1C), where no gall smaller than 3.50 mm in diameter was parasitized. Although larger, attacked galls were associated with a negative effect on gall wasp survival. We dissected 51 B. treatae galls attacked by C. filiformis and 23 had a dead ‘mummified’ adult B. treatae inside (45%). For the 101 B. treatae galls not attacked by C. filiformis, we found only 2 individuals with dead adult B. treatae (2%; all other galls possessed an emergence hole made by either the gall wasp or natural enemy). The difference in the proportion of dead wasps associated with C. filiformis attack was highly significant R864
among all galls (2=45.85, P<0.0001; Figure 1D), even after limiting our comparison to galls of a similar size (by dropping all galls below 3.5 mm in diameter; 2=28.02, P<0.0001), suggesting that C. filiformis has an important negative impact on gall wasp survival. Consistent with this being a potentially general, but previously unrecognized, trophic interaction, C. filiformis haustoria were observed directly attacking a large multichambered stem swelling gall induced by a second, but less abundant, gall-forming wasp, Callirhytis quercusbatatoides, at the same site in southern Florida (Figure S2A,B). Of the 65 galls surveyed, attack of C. quercusbatatoides was observed 11 times (17%), with a range of one to five haustoria connected to a single gall (mean=1.50±0.44 SE). Once again, C. filiformis parasitism was associated with a modified gall phenotype. Here, C. quercusbatatoides galls attacked by the vine were 13.5% smaller (n=11; mean diameter for parasitized galls ± SE=14.41±0.64 mm) than non-parasitized galls (n=54; mean diameter for galls not parasitized ± SE=16.65±0.47 mm; t=2.07; P=0.043). In addition, C. filiformis was found in association with five other gall-forming species, including two wasps that induce galls on the bottom of new leaves (Andricus quercuslanigera, Neuroterus minutissimus), where C. filiformis were also found to form haustoria. In addition, C. filiformis was found in association with five other gall-forming species. This included two wasps that induce galls on the bottom of new leaves (Andricus quercuslanigera, Neuroterus minutissimus), where the vine was also found to form haustoria, and two wasps (Disholcaspis quercusvirens, A. quercusfoliatus) and one gall forming fly (Arnoldiola atra [Cecidomyidae: Diptera]) that manipulate stems or buds, where the vine was observed to wrap tightly, multiple times, directly below the gall and initiate haustoria into the stem tissue (Figure S2C). Is this truly a new trophic interaction? Certainly, it is well documented that carnivorous plants can consume insects directly [8], and there is evidence that parasitic plants can indirectly alter host plant interactions
Current Biology 28, R847–R870, August 20, 2018
with other herbivorous community members [9,10]. There is also evidence that other guilds of parasitic wasps (such as inquilines) can attack and manipulate the gall formation process, sometimes killing the gall former [3]. However, this is the first report of a parasitic plant directly attacking an insect-induced plant structure that negatively impacts the insects’ fitness and/or survival. How common is this new trophic interaction in nature? The potential is global in scale, as parasitic plants comprise 1% of angiosperm diversity (~4,500 species in 20 families) [5] and gall formation has been described in over 13,000 species in six insect orders [2,3], and both live in almost every terrestrial habitat on Earth. SUPPLEMENTAL INFORMATION Supplemental Information contains two figures and experimental procedures, and can be found with this article online at https://doi. org/10.1016/j.cub.2018.06.024. REFERENCES 1. Futuyma, D.J., and Agrawal, A.A. (2009). Macroevolution and the biological diversity of plants and herbivores. Proc. Natl. Acad. Sci. USA 106, 18054–18061. 2. Stone, G.N., and Schönrogge, K. (2003). The adaptive significance of insect gall morphology. Trends Ecol. Evol. 18, 512–522. 3. Stone, G.N., Schönrogge, K., Atkinson, R.J., Bellido, D., and Pujade-Villar, J. (2002). The population biology of oak gall wasps (Hymenoptera: Cynipidae). Annu. Rev. Entomol. 47, 633–668. 4. Dawkins, R. (1982). The Extended Phenotype: The Long Reach of the Gene (New York: Oxford). 5. Westwood, J.H., Yoder, J.I., Timko, M.P., and Depamphilis, C.W. (2010). The evolution of parasitism in plants. Trends Plant Sci. 15, 227–235. 6. Egan, S.P., and Ott, J.R. (2007). Host plant quality and local adaptation determine the distribution of a gall-forming herbivore. Ecology 88, 2869–2879. 7. Egan, S.P., Hood, G.R., and Ott, J.R. (2011). Variable selection on gall size: differential contributions of individual host plants to population wide patterns. Evolution 65, 3543–3557. 8. Cameron, K.M., Wurdack, K.J., and Jobson, R.W. (2002). Molecular evidence for the common origin of snap-traps among carnivorous plants. Am. J. Bot. 89, 1503–1509. 9. Press, M.C., and Phoenix, G. K. (2005). Impacts of parasitic plants on natural communities. New Phytol. 166, 737–751. 10. Manrique, V., Cuda, J.P., Overhold, W.A., and Ewe, S.M.L. (2009). Synergistic effect of insect herbivory and plant parasitism on the performance of the invasive tree Schinus terebinthifolius. Entomol. Exp. Appl. 132, 118–125.
Department of BioSciences, Rice University, Houston, TX 77005, USA. *E-mail: [email protected]