Research Article |
Corresponding author: Anthony Bain ( anthonybain22@mail.nsysu.edu.tw ) Academic editor: Petr Janšta
© 2019 Da-Mien Wong, Anthony Bain, Shiuh-Feng Shiao, Lien-Siang Chou.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Wong D-M, Bain A, Shiao S-F, Chou L-S (2019) Fighting injuries, fig exit, and dimorphism in two species of sycoryctine fig wasp (Chalcidoidea, Pteromalidae). Journal of Hymenoptera Research 74: 105-121. https://doi.org/10.3897/jhr.74.36461
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Similar to many vertebrate and invertebrate species, many fig wasp species are fighting other members of their species for mates. Fighting between the males of many non-pollinating fig wasp species involves injuries and fatalities. Studies have shown that large males fight for mates, whereas conspecific small males tend to adopt nonfighting, sneaky behaviors. To analyze male morphs in two non-pollinating fig wasps (Philotrypesis taida Wong & Shiao, 2018 and Sycorycteridea taipeiensis Wong & Shiao, 2018) associated with the fig tree Ficus benguetensis, the head and mandible allometry and injuries were examined as well as the morphologies of their heads and mandibles. Male fig wasps of these two nonpollinating species can be divided into two morphological groups according to their head and mandible shapes. Approximately 88% of the Philotrypesis and 62% of the Sycorycteridea males were injured and no males belonging to largest morphs were decapitated. Moreover, nearly 31% of the Philotrypesis and 45% of the Sycorycteridea males left their natal figs. No difference in injury level or male exit rate between the male morphs was observed. This study reveals slight morphological and behavioral differences that may hint towards different mating strategies among morphs.
Ficus benguetensis, fatal fighting, male dimorphism, male dispersal, Philotrypesis, Sycorycteridea
Fighting is ubiquitous in the animal kingdom (
Fig. wasps are small insects that are obligately associated with plant of genus Ficus (
Fighting among male fig wasps occurs in both pollinating and non-pollinating species (
The aim of this study was to document morphological variations, the fighting outcomes, and the exit rates of two species of non-pollinating fig wasp living on Ficus benguetensis. Preliminary observations of Philotrypesis taida Wong & Shiao, 2018 and Sycorycteridea taipeiensis Wong & Shiao, 2018 males had revealed that: (1) males are fighting inside the figs, (2) fighting may result in death by decapitation, (3) males vary in size, and (4) males may exit figs. On the basis of these observations, this study raised the following questions concerning male interactions among the studied species: (1) How different in size and morphology are these males? (2) How common are injuries and fatal injuries? (3) How often do males exit their natal figs? (4) What are the factors (e.g., fig diameter linked with the fighting space, sex ratio linked with the number of fighters) affecting the level of injury and the exit rate?
Philotrypesis taida and Sycorycteridea taipeiensis belong to the Sycoryctinae subfamily (Chalcidoidea: Pteromalidae) and are the two non-pollinating fig wasp species associated with the gynodioecious Ficus benguetensis Merrill (
Thirty ripe unexited figs were haphazardly collected from five F. benguetensis trees in Taiwan from October 2011 to July 2012 (see Suppl. material
The collected Philotrypesis and Sycorycteridea males were examined for their fighting injuries. All observed lacerations and amputations were noted. The injury level of an individual male was estimated according to a rating scale developed for fighting fig wasps (
Score | Description |
1 | Loss of part or whole tarsus |
1 | Loss of part or whole mandible |
2 | Loss of part or whole antenna |
2 | Loss of part or whole tibia |
3 | Loss of part or whole femur |
4 | Loss of part or whole coxa |
4 | Laceration in abdomen |
8 | Decapitation |
Male exit was estimated as the proportion of males exiting their natal fig, namely the “male exit proportion”, and was calculated as the number of exited males divided by the total number of males per fig.
The sex ratio for each species was calculated as the number of male wasps divided by the total number of wasps within a fig. All statistical tests were performed using the R 3.6.1 statistical software (
One hundred eighty-two Philotrypesis and 42 Sycorycteridea male wasps were collected. The average sex ratio of the sampled figs was 0.36 ± 0.03 for Philotrypesis and 0.47 ± 0.09 for Sycorycteridea, which was significantly different from the 1:1 ratio for Philotrypesis (t = 4.44, df = 48, P < 0.001) but not for Sycorycteridea (t = 0.39, df = 22, NS). The sex ratio of the two species was not different (t = -1.16, df = 14.03, NS).
Two Philotrypesis male morphologies, namely “atypical” and “typical” morphs, were identified. They were distinguished by the shapes of their mandibles (Fig.
Frontal view of the males of the two studied species and mandible outline (a) a “typical” Philotrypesis male: rounded back of the head and broad mandibles (b) “atypical” Philotrypesis male: head more square and falcate mandibles (c) Sycorycteridea small male, rectangular head (d) Sycorycteridea large male, lantern-shaped head.
Morph | N | Mean head width | Head width range | Mean mandible length | Mandible length range | |
Philotrypesis | Atypical | 13 | 0.673 ± 0.187 a | 0.550–0.719 | 0.323 ± 0.089 | 0.242–0.370 |
Typical | 169 | 0.576 ± 0.044 b | 0.366–0.675 | 0.233 ± 0.018 | 0.134–0.310 | |
Sycorycteridea | Large | 18 | 0.502 ± 0.118 c | 0.453–0.562 | 0.290 ± 0.068 | 0.243–0.326 |
Small | 24 | 0.336 ± 0.069 d | 0.215–0.388 | 0.153 ± 0.031 | 0.078–0.230 |
The mandible length of Philotrypesis males correlated positively with head width (Spearman rank correlation test: ρ = 0.759, df = 180, P = 2.58E-35; Fig.
The number of Philotrypesis males of each morph in each injury level was not different (χ²1 = 0.48, NS), same for the Sycorycteridea morphs (χ²1 = 0.00, NS; Table
Philotrypesis | Sycorycteridea | |||
typical (N = 169) | atypical (N = 13) | small (N = 24) | large (N = 18) | |
Uninjured (injury score = 0) | 0.11 | 0.15 | 0.29 | 0.50 |
Minor (injury score <8) | 0.46 | 0.31 | 0.50 | 0.33 |
Severe (injury score ≥8) | 0.43 | 0.54 | 0.21 | 0.17 |
Mean injury score per individual and injury proportion distributed among different body parts.
Philotrypesis | Sycorycteridea | |||
typical (N = 169) | atypical (N = 13) | small (N = 24) | large (N = 18) | |
Mean injury score | 7.4 ± 0.6 a | 7.1 ± 2.0 a | 3.8 ± 0.8 b | 3.5 ± 0.8 b |
Abdomen | 0.01 | 0.00 | 0.00 | 0.00 |
Antenna | 0.37 | 0.62 | 0.25 | 0.28 |
Coxa | 0.31 | 0.23 | 0.21 | 0.11 |
Decapitation | 0.08 | 0.00 | 0.04 | 0.00 |
Femur | 0.49 | 0.46 | 0.25 | 0.22 |
Tarsus | 0.42 | 0.38 | 0.29 | 0.22 |
Tibia | 0.32 | 0.46 | 0.17 | 0.22 |
Philotrypesis had a significantly higher LEI value (t = 3.11, df = 35, P < 0.01; Table
Average numbers per fig and injury rates for the two non-pollinating fig wasp species (N = 30 figs).
Philotrypesis | Sycorycteridea | |
Mean wasp number | 21 ± 5 | 12 ± 3 |
Male exit rate | 0.31 ± 0.06 | 0.45 ± 0.13 |
Lifetime Extent of Injury (LEI) | 5.6 ± 0.6 a | 2.5 ± 0.7 b |
Proportion of injured males (IF) | 0.88 ± 0.02 a | 0.62 ± 0.07 b |
Severe Injury Frequency (SIF) | 0.23 ± 0.03 | 0.10 ± 0.05 |
The calculation of the injury score differs from
Most of the male fig wasps exited within 2 h after the first wasp had emerged from the fig. No difference in the proportion of exited males was observed between the two non-pollinating species (χ²1 = 0.00, NS; Table
The multiple linear regression model contained five variables (average head width, fig diameter, LEI, morph ratio, and sex ratio) was significant, showing that the five variables collectively explain the exit rate. In addition, the average Philotrypesis male head width was the main contributor of the model (Table
Result of the multiple linear regression model with the male exit proportion as dependent variables.
Philotrypesis (R2 = 0.47* F = 3.37) | Sycorycteridea (R2 = 0.52 F = 1.28) | |||
β | t | β | t | |
Average head width | 4.05 | 2.36* | 1.15 | 0.28 |
Fig. diameter | -0.02 | -1.40 | -0.01 | -0.22 |
LEI | -0.02 | -0.85 | -0.07 | -1.12 |
Morph ratio | -0.49 | -1.09 | -0.48 | -0.67 |
Wasp sex ratio | -0.32 | -0.90 | -0.93 | -1.61 |
Our results show that the males of each of the two studied species had two clearly defined morphs. The Philotrypesis males could not be categorized according to their size only because some of the atypical males were smaller than the largest typical male: The shapes of the heads and mandibles were the discriminative morphological features. The shapes of the head and the mandibles were also discriminative for the morphs of the Sycorycteridea males but these males could also be segregated according to their size only. Such dimorphism (discontinuous distribution of male size) has never been observed before in male fig wasps. Moreover, injuries were found in every morph of both species, and it seems that belonging to a specific morph does not affect the probability of injury. Nevertheless, morph type may affect the severity of injury; no decapitated males belonging to the atypical Philotrypesis or large Sycorycteridea morphs were found in this study. However, the absence of decapitated males could be a random effect of the sampling as only the little number of atypical Philotrypesis has been found.
In contrast to other Philotrypesis species (
The Sycorycteridea morphs in this study were uniquely morphometrically defined; no continuous distribution of mandible length or head width was noted, in contrast to Australian Sycoscapter species living on F. macrophylla (
The injury frequencies (IF) of P. taida and S. taipeiensis in this study are the highest ever documented in any non-pollinating fig wasp species (88% and 62% for Philotrypesis and Sycorycteridea respectively). In congeneric species, very few fight winners were injured, whereas 22% of Philotrypesis losers and 73% of Sycorycteridea losers were injured (
Although studies on the dispersal (exit from a natal fig) of non-pollinating wingless male fig wasps are extremely limited, the few published studies have revealed a wide range of exit rates; 27%–71% of males of non-pollinating fig wasp species living in F. ingens figs exit their native figs (
Considering the high probability of being captured by ants (
The findings of this study confirm the type of dimorphism that has been described in other Philotrypesis species and reveal a new dimorphism type in the Sycoryctinae subfamily. Some intermorph values found in this study could be used as insights for behavioral differences between morphs related to aspects such as fighting or exiting figs. Our research provides basic information that could lead to behavioral studies of these males and the environmental factors that may affect the choices of fig wasp mothers to produce any morph at an oviposition site.
The authors thank Prof. Tzeng Hsy-Yu from National Chung Hsing University for generous guidance on study methods. The authors would also like to express deepest appreciation to Prof. Hsu Yu-Ying and Prof. Yang Jeng-Tze from National Taiwan Normal University and National Chung Hsing University, respectively, for their valuable suggestion and discussion. This research is supported by National Science Council of Taiwan (99-2923-B-002-001-MY3).
Table S1. Thirty sampled figs were haphazardly collected from Ficus benguetensis trees within five natural habitats of Taiwan
Data type: species data
Figures
Data type: multimedia
Explanation note: Figure S1. The heads from two Philotrypesis taida individuals. Figure S2. Cluster of Ficus benguetensis figs in the National Taiwan University campus, Taipei, Taiwan.