Philippa Kaur

Affiliations

Department of Biology, University of Miami, Coral Gables, FL, USA
K. J. Feeley, C. Bravo-Avila, B. Fadrique & T. M. Perez

Fairchild Tropical Botanic Garden, Coral Gables, FL, USA
K. J. Feeley, C. Bravo-Avila & T. M. Perez

Universidad Nacional de Colombia Sede Medellín, Medellín, Colombia
D. Zuleta

Forest Global Earth Observatory, Smithsonian Tropical Research Institute, Washington DC, DC, USA
D. Zuleta

Authors
K. J. Feeley

C. Bravo-Avila

B. Fadrique

T. M. Perez

D. Zuleta

Corresponding author
Correspondence to K. J. Feeley. More

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. More

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Trabaque tufa record
Trabaque Canyon (40.36° N; 2.26° W; 840 m above sea level) is located in the central Iberian Peninsula (Fig. 1). At this site, tufa deposits precipitate as freshwater carbonates downstream of overflow karst springs. During the last interglacial period, tufa precipitated continuously at the studied site while water level of the aquifer was high enough for upstream springs to discharge13. Outcrops of the studied tufa deposit are preserved in the margins of Trabaque River over a distance of 500 m downstream of overflow karstic springs. The studied tufa deposit is 12 m thick, with a gentle ramp morphology, and a simple stratigraphy of sub-horizontal tufa beds that covered the full section of the narrow canyon. The accumulation of tufa created a small lake upstream the ramp, which prevented erosive events while the deposit was active, because most of the river bedload was accumulated in the basin of the lake. This configuration favoured the lack of erosive episodes in the tufa and the deposition of a continuous record. The tufa deposit was partially eroded by subsequent fluvial incision once the tufa accretion ceased and detrital sediments filled the lake basin and started to flow over the ramp during floods. The tufa deposit is mostly composed of well-cemented intra-clastic and peloidal carbonate particles13. The deposit comprises tufa beds 0.02–1 m thick that typically extend tens of metres downstream. At the base of the section, the tufa lies over loose fluvial sediments of sandy silt, whereas at the top of the section there is an erosive scar, and recent gravitational deposits overlay the tufa preserved in the slopes of the canyon.
Figure 1

Pictures of Trabaque Canyon and the studied deposit. (a) Trabaque Canyon. The river flows according to yellow arrows. The red ellipse shows the location of the main section where the deposit was sampled. The inlet map shows the location of Trabaque Canyon within the Iberian Peninsula. (b) View of most of the studied Trabaque tufa section. The base and top of the section are missing from this panorama. The centre of the valley bottom is to the left of the image and the slope of the canyon to the right. The river flowed from the position of the observer towards the tufa deposit. The picture shows gravitational pulses GP-2 and GP-3 that interdigitate with the tufa deposit, and their disappearance from the bottom of the valley after GP-3. (c) Detail of GP-3 gravitational deposit. (d) Detail of the alternation between well-cemented and loose tufa beds at the top of the section.

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The base of the deposit section is characterized by nearly 4 m of tufa sediments in the centre of the valley, laterally interdigitating with gravitational deposits towards the slopes (Fig. 1). These gravitational deposits partially invaded the bottom of the valley during three distinct pulses. These gravitational deposits occurred during periods of enhanced slope processes due to the decrease in vegetation cover on the canyon slopes during prolonged dry periods. The evidence of local erosion recorded by the gravitational deposits is consistent with other proxies that record local and regional erosion and that are displayed in Fig. 2. Thus, independent evidence of erosion is also recognized from the increase of insoluble residue (IR) particles in the tufa, recorded by the percentage of silt IR. IR particles were transported to the tufa by the river or by the action of wind. The increase of these particles in the tufa is interpreted as enhanced erosion, not only from the catchment but also from outside the basin. Higher concentrations of Si and Al are also interpreted as proxies of soil erosion from areas with silicate substrates inside or outside the catchment. The increase of micro-charcoal particles in the tufa is also interpreted as a sign of enhanced soil erosion. Charcoals were incorporated to the tufa during floods or transported by the wind after the occurrence of fires, as well as from the erosion of soils that accumulated charcoals from previous fire events. In any case, the increase of micro-charcoals in the tufa record suggests soil erosion due to the lost of vegetation cover. Major events of local and regional erosion occurred synchronously (Fig. 2), supporting that the common decreases in vegetation cover that resulted in erosion events were related to periods of reduced precipitation.
Figure 2

Record of the Trabaque tufa deposit. (a) Simplified lithological log of the Trabaque record. Patterns represent gravitational deposits (black) with distinct three pulses, well-cemented tufa sediments (light grey), and alternation of well-cemented and loose tufa sediments (dark grey). (b,c) Tufa δ18O and δ13C records. Isotope values at each date (dots) are the average of 3 sub-samples and blue/red line is a 3-point running mean. The grey shade shows the 1σ variability of the three sub-samples along the record. (d) Concentration of Si and Al. (e) Silt-sized insoluble residue in tufa as percentage of the total sample. (f) Counts of micro-charcoal particles  More

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General situation of the research area
The research area was conducted at Liufangzi village, Gongzhuling city, Jilin Province (N43°34′10″, E124°52′55″), as shown in Fig. 8. The area has a continental monsoon climate in the humid area of the middle temperate zone, with an average annual precipitation of 594.8 mm, which is mainly concentrated in June and August. The average annual temperature is 5.6 °C, and the daily average temperature drops to 0 °C in November of each year, with a freezing period of up to five months. Corn is one of the main commodity crops in the area, with a sowing date in early May and a harvest date in early October.
Figure 8

Location of study area (Liufangzi Village, Gongzhuling City, Jilin Province).

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The soil of the site is a silty loam black soil, which had been planted with monoculture corn with no tillage for 5 years. On October 5, 2018 (after the autumn harvest), a flat field was selected to set up the experiment. Soil samples were collected using the zigzag sampling method, and selective physical and chemical properties of soil were determined, including pH (5.48), organic matter (26.4 g kg−1), clay (29.12%), and soil bulk density (1.21 g cm−3 in 5–10 cm and 1.53 g cm−3 in 20–25 cm).
Reagents and instruments
Reagents
The main raw material of the added impervious agent was corn starch and acrylic compound, which was entrusted to Jilin Yida Chemical Co., Ltd. The added urea was an analytical reagent, and the reagents used for analysis included H2SO4, H3PO4, NaOH, NH4OH, NH4Cl, K2S2O8, Na2B4O7, KNO3, KNO2, K2Cr2O7, FeSO4, sulfonamide, and naphthalene ethylenediamine hydrochloride; these were all analytical reagents provided by Beijing Chemical Plant.
Instruments laboratory-built soil leaching column; continuous flow injection analyser (SKALAR SA++, Netherlands).
Test plot setup and agronomic practices
The experimental plots were maintained in the field consisting of (1) CK (no-tillage control treatment, with corn straw removed and soil left under no-till management); (2) ploughing treatment (corn straw was removed and then mouldboard ploughed to a 30 cm depth); (3) straw returning treatment (corn straw (25.32% moist) was incorporated into the soil on October 5, 2018 (after autumn harvest), with an application amount of 1.25 kg m−2. Briefly, corn straw was chopped into small pieces (0.5 cm length), evenly placed on the soil surface, and then incorporated into the soil with ploughing (the depth of 30 cm)); and (4) impervious agent addition treatment (the impervious agent mentioned previously evenly laid on the soil surface at the amount of 15 g m−2 and then incorporated into the 0–30 cm soil by mouldboard ploughing). The abovementioned field operations were conducted after corn harvest in the fall of 2018 with a testing area of 10 m × 50 m for each plot and three replicates for each treatment. In the following spring (2019), grain corn was planted in all treatment plots with a planting density of 65,000 plants ha−1. All plots were managed in the same way with a one-time fertilization application of 200–90-90 kg (N-P-K) ha−1 and 2,4-d spray as weed control.
For all the above treatments (including the control treatment), undisturbed soils (0–30 cm layer) were collected with an undisturbed soil column (refer to Fig. 9) for the leaching experiment on September 25, 2019 (before autumn harvest, after 350 days of straw returning to the field); soil samples of 0–15 cm were collected for determination of soil organic matter and adsorption experiment of nitrogen in the soil; and soil samples of 5–10 cm and 20–25 cm layers were collected for determination of soil bulk density. In addition, for the straw returning treatment, one sampling was added on May 25, 2019 (one month after sowing, 230 days after straw returning), for the determination of soil organic matter content and soil bulk density, nitrogen adsorption and leaching experiment in soil.
Figure 9

Schematic diagram of simulated leaching device of undisturbed soil column. (a) Soil extraction; (b) leaching; (c) physical map of leaching in undisturbed soil column. 1: Handle; 2.3.4: guide port; 5.6: screw port; 7: punching plate. I main body of leaching column; II soil cutter; III leaching solution collector.

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The soil samples used for soil organic matter determination and nitrogen absorption testing were air dried, sieved through a 2-mm sieve and visible plant debris and stones were removed, and then stored.
Experiment of nitrogen adsorption in soil
Ten parts of the soil samples (air-dried,  More

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