NPFWs are generally considered to have negative effects on the fig tree–fig pollinator mutualism according to theoretical studies2,4,6. Many empirical and experimental studies have justified this conclusion. Some studies show that NPFWs have a negative effect and found a negative correlation between the offspring number of NPFWs and the offspring number of pollinator and seeds9,13,14. For instance, Patel19 found no correlation between the offspring number of pollinator and NPFWs in their survey , and Peng et al.20 recorded a positive correlation between the offspring number of NPFWs and pollinator in figs of F. hispida . Our capacity to detect the real cost of development of different types of NPFWs and their exact effect on the mutualism is limited by many interaction factors13 and non-experimental empirical studies can underestimate or fail to detect the impact of NPFWs on this obligate mutualism when overall consideration was taken with different studies of pollinator-NPFW interactions in consideration18.

For early-ovipositing gallers, a remarkable feature of those species is that their galls usually fill the space of B-phase syconium cavities and can greatly hinder pollinator movement and oviposition, thus result in their specific consequences on the mutualism24. For example, Conchou et al.13 studied Ficicola spp. which is a genus of early-ovipositing large-sized gallers hosted by F. guianensis and found a substantial negative impact of this genus on the production of both pollinators and seeds. Here, we present another case that studies the effect of an early gall inducer.

Our study has explored the effect of early-ovipositing gallers on the growth of figs (fig size of matured figs) for the first time. In our study, it turns out that early-ovipositing gallers can greatly depress the growth of the figs. The mechanical injury caused by the insertion of the ovipositor of S. testacea to the tiny figs may be responsible for the depression of the growth of the Fig25. Another possible reason is the gall-inducing process26. Jansen-González26 et al. studied the gall-inducing process and larval feeding strategy of pollinating and non-pollinating fig wasp species associated with F. citrifolia and found that the way non-pollinating galler induces gall is quite different from pollinators and they exploit plant resources more aggressively26. With the involvement of the pollinators, the growth of figs improved greatly. The existence of both seeds and larvae of the pollinator, both of which is essential to the fitness of fig trees, may contribute to the improvement of the growth of the figs.

The variation trend of development ratio is consistent with fig volume, which can be explained by the saction mechanism applying to uncooperative cheaters27,28,29,30,31. Jander et al.27,28,29 found that the Ficus tree can sanction the pollen-free pollinators through decreasing their offspring development ratio and increasing the abortion rate of the unpollinated figs. Almost all the non-pollinating figs wasp species lay their eggs in the female flowers but not spread pollen to the fig, which is analogous to the cheaters of pollinators. It makes sense that the same sanction mechanism works on the non-pollinating fig wasps. When only S. testacea oviposit in the fig, most of the figs aborted, and the fig tree invests little nutrition for the remaining figs that survived. With the increase of oviposition and pollination by pollinators (2Cf + St treatments versus St treatment), and the decrease of mechanical injury by NPFWs (2Cf treatments versus St treatment), fig trees invest more nutrition to those figs and the development ratio of the galls increases. Jander et al.28 argued that sanctions can be modular or individual. In a modular sanction, all the offspring produced in the fruit is punished due to involvement of non-cooperative individuals. Our experiment can be a good test of this hypothesis as we can investigate accurately the development of the pollinator and the cheater (S. testacea) respectively. By comparing the theoretical value and the actual number of galls for 2Cf + St treatment, we can explore the source that leads to the decrease of the overall development ratio in the 2Cf + St treatment compared with the 2Cf treatments, thus determine if the sanction works at fig level (modular) or not. We found there is no significant difference between theoretical value and the actual number for 2Cf + St treatment, which suggests that the development ratio of the two species is independent of each other, so the lower development ratio of 2Cf + St treatment compared with 2Cf treatment was caused mainly by the low development ratio of S. testacea. For 2Cf + St treatment, the development ratio of pollinator didn’t decrease, and being pollinated didn’t change the development ratio of S. testacea, which means pollination didn’t increase the nutrition provided to galls of. S. testacea. Our results show that the sanction is not at a fig level, which is inconsistent with the sanction to the cheaters in pollinators (pollen-free pollinators)28,30. Perhaps the sanction mechanism is related to the identification of the cheaters. When the host can identify the cheaters, the sanction can work at individual level where they may only sanction the offspring of cheaters, such as S. testacea in this study. If the host can’t identify the cheaters, the sanction may work at fig level (modularly) through sanctioning all the wasps reproduced in the fig, such as the cheaters in the pollinators.

The production of seeds is influenced greatly by the wasp S. testacea. A former study shows that galls produced by early-ovipositing gallers often fill B-phase syconium cavities and hinder pollinator movement and oviposition24, which can explain the decline of the seed production. In our study, the oviposition behavior of pollinators was much less affected than the pollen spreading behavior due to the block of galls produced by S. testacea.

For the treatments with the pollinators, figs with S. testacea (2Cf + St treatment) have more galls than figs without S. testacea (2Cf treatment). This indicts that the existence of galls produced by S. testacea has little effect on the egg-laying behavior of the pollinator. Since pollinators lay their eggs in the female flowers one by one and the number of eggs to be laid is much less than the number of pollen to be spread, it’s easy to understand that oviposition is less affected than pollen spreading.

Our study shows that S. testacea has an obvious negative effect on the fig tree-fig pollinator mutualism. Oviposition by S. testacea leads to a drastic decrease in seed production, thus may harm the maintenance of stability of fig tree-fig pollinator mutualism if the fig is excessively parasitized by S. testacea. We think the mechanical injury from oviposition, the galling process, and the blocking of cavity by the galls of S. testacea may be responsible for the negative consequences. For figs in which only S. testacea oviposit, the total galls are much less than figs in which pollinators were introduced. There are two possible reasons. One possible reason is that the low density of the population of S. testacea results in the low oviposition rate. Another possible reason is that the fig tree may sanction the unpollinated figs, ie, the figs in which only S. testacea oviposit. Wang et al.30,31 found that the sanction mechanism also works on F. racemosa. Further more, they found that the sanction strength became stronger with an increase in foundresses30 (the wasps that enter the figs to oviposit). If too many S. testacea oviposit in figs, the figs are aborted more easily due to sanction by the tree. Only figs that contain a small number of galls survive.

Although many studies9,11,13,14,15,16,17,18 have shown that NPFWs can have a negative effect on the fig tree-fig pollinator mutulism due to the reduction in pollinator offspring or the seed production, some study has found that the NPFWs also can play a positive role in maintaining the stability of this obligate mutualism32. For example, parasites may stabilize and maintain the fig and fig wasp system through their effects on within- and between-tree reproductive phenology32. More specifically, oviposition by NPFWs can result in the asynchrony of the development of the figs, and increase the probabilities of pollinators finding oviposition sites, which is good for the maintenance of this mutualism32.

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