Turning lances into shields: Flower mantids stretch their raptorial forelegs to avert and deflect predator attack

Li, Yuanlang 1 ; Liu, Qinpeng1; Chen, Zhaoyang1; Liang, Le2; Wang, Zhixin1; Duan, Yuange1; Song, Fan1; Cai, Wanzhi1; Ge, Jin3; Li, Hu1; Tian, Li1

Published Feb 27, 2025; Updated Mar 03, 2025 on Dryad. https://doi.org/10.5061/dryad.3xsj3txq1

Abstract

Evolutionary co-option, in which existing traits acquire novel adaptive functions, is a key strategy by which organisms adapt to new environmental challenges. Although such co-option has been widely documented at the genetic and morphological levels, its incidence at the behavioural level remains largely unknown. Mantids stretch their forelegs to capture prey; however, some flower mantids also perform foreleg stretches in the absence of prey. The current study tested whether this behaviour represents a novel function of the foreleg stretch, thus representing a case of behavioural co-option. Predator encounter behaviour assays revealed that foreleg stretching facilitates the escape of flower mantids from large predatory mantids by delaying predator approach or deflecting their attack towards less vulnerable body parts. Phylogenetic analysis suggested that the ancestral function of foreleg stretching involves prey capture, with the anti-predator function subsequently acquired in the flower mantid clade, coinciding with the diversification of large-sized mantids, the most likely invertebrate predators of flower mantids. This study provides a case of behavioural co-option, where a predator uses its predatory organ as a defensive implement to cope with its own predators. These findings further suggest that behavioural co-option may be common in nature, meriting more comprehensive studies.

https://doi.org/10.5061/dryad.3xsj3txq1

Contact Yuanlang Li (lyls71120@163.com) with any questions. This manuscript has been accepted for publication at Proceedings of Royal Society B.

Li Y, Liu Q, Chen Z, Liang L, Wang Z, Duan Y, Song F, Cai W, Ge J, Li H, Tian L. Turning lances into shields: flower mantids stretch their raptorial forelegs to avert and deflect predator attack. Proc. R. Soc. B (accepted). 10.1098/rspb.2024.3081

Description of the data and file structure

Files and variables

File: DataS1.csv

Description: Data from Predator encounter assay, including normal groups and manipulated group.

Variables

Predator IDs: Predator identity number
Flower mantid IDs: Flower mantid identity number
If stretching: Flower mantid stretching or not
Targets: Predator’s targets
Outcomes: Outcomes of the Predator encounter assay
Treatments: Control or Forelegs-disabled

File: DataS2.csv

Description: Data from Predator encounter assay, showing deviation angles of predators’ head before and after foreleg stretching.

Variables

Before : Deviation angles (deg) of predators’ head before foreleg stretching
After : Deviation angles (deg) of predators’ head after foreleg stretching

File: DataS3.csv

Description: Data from Predator encounter assay, showing predators’ speed when they are approaching the flower mantids.

Variables

Event IDs: Event identity number
Time since prey detection (sec): Time since prey detection
Distance (mm): Distance between predator and flower mantid

File: DataS4.csv

Description: Data from Characterising the types of foreleg stretching behaviours.

Variables

Behaviour IDs: Behaviour type’s identity number
Point IDs: Point identity number
x (mm): X-axis coordinate
y (mm): Y-axis coordinate

File: DataS5.csv

Description: Data from Morphometrics of foreleg femurs, including the morphological data of foreleg-femurs of 16 adult A. *basinigra *specimens.

Variables

Specimen IDs: Specimen identity number
Sex: Sex of specimen
Length (mm): Length of foreleg-femurs
Width (mm): Width of foreleg-femurs
Thickness (mm): Thickness of foreleg-femurs

File: DataS6.csv

Description: Data from Morphometrics of foreleg femurs, including the morphological data of foreleg-femurs of selected 93 specimens from 7 Hymenopodidae species.

Variables

Species: Scientific names of selected Hymenopodidae species
Specimen IDs: Specimen identity number
Sex: Sex of specimen
Femur length (mm): Length of foreleg-femurs
Femur width (mm): Width of foreleg-femurs
Relative width: Femur width/Femur length (dimensionless number)

File: DataS7.csv

Description: Data from Frequency measurement of behaviour.

Variables

Resting: Stretching times per minute when mantid in ‘resting’
Moving: Stretching times per minute when mantid in ‘moving’

File: DataS8.csv

Description: Data from Speed comparison between control and treatment group.

Variables

Mean.speed.CK: Mean speed (mm/s) of control group

Mean.speed.TR: Mean speed (mm/s) of treatment group

File: glmm.data.xlsx

Description: Data for GLMMs, original record see DataS1.csv.

Variables:

predator_id: Predator identity number
prey_id: Flower mantid identity number
experience: The number of encounters of predator with flower mantid
prey_stretching: Flower mantid stretching or not ("1", stretching; "0", non stretching)
escape: Experiment outcome ("1", Escape; "0", Capture)

File: Chisq.test.data.txt

Description: Data for chisq-test, original record see DataS1.csv.

File: linear.regression.data.txt

Description: Data for linear regression, original record see DataS3.csv.

Variables:

Stretching: Stretching or not ("1", non stretching; "2", stretching)

Time: Time since prey detection (sec)

Distance: Distance between predator and flower mantid (mm)

File: DNA_Information.pdf

Description: DNA sequences information

Information:

Species: Scientific names of species
Accession number: NCBI number

Collection information: Collection information of specimens

File: Mantidea_state_matrix.csv

Description: Data for phylogenetic analyses.

Information:

Species: Scientific names of selected Hymenopodidae species
x: Behavioural state

File: hymenopodidae_Mantidae.csv

Description: Supporting file for Species_Distribution_and_Point_Data

Information:

Longitude: Longitude position
Latitude: Latitude position
family: Taxonomic rank ("Mantidae" or "Hymenopodidae")

Codes information

The following four files include the R codes used in this article. For more detailed information, please refer to our code annotations, main text, and supplemental materials (DOI: 10.1098/rspb.2024.3081).

R Studio software, v. 2024.09.1+394, R software, v. 4.2.2 (R Core Team, 2024)

Statistical.Codes

R codes for statistical analysis. Including:

(1) regarding GLMMs and Chisq-tests for Predator encounter assay (Based on DataS1);

(2) t-test for Frequency measurement of behaviour (Based on DataS7);

(3) t-test for Deviation angle of predator's head (Based on DataS2);

(4) t-test for Speed comparison between control and treatment group (Based on DataS8);

(5) linear regression for The change in relative distance between predators and flower mantids over time (Based on DataS3).

Reconstruction_of_Ancestral_States_and_rate_change_across_time

R codes for Divergence time estimation and ancestral state reconstruction.

Mantidea_pruned_outgroups.tree

Phylogenetic tree file.

Species_Distribution_and_Point_Data

R codes for generating species distribution maps (see Figure S1).

Version changes

5-Mar-2025:

(1) Provided new data files (including glmm.data.xlsx, Chisq.test.data.pdf, and linear.regression.data.txt) for statistical analyses.

(2) Revised DataS2, DataS7, and DataS8 for statistical analyses. The changes only involve formatting and column names to facilitate statistical analyses; the original data remains unchanged.

(3) Provided supporting file (hymenopodidae_Mantidae.csv, and Mantidea_state_matrix.csv) for statistical analysis.

Please note that this version does not modify any of the original data.

Predator encounter assay

We performed predator encounter assays using 4th instar nymphs of the flower mantid Astyliasula basinigra (n = 26) as the model and 4th instar nymphs of the large-sized mantid Rhombodera longa (n = 9) as the predator.Results showed that:

(1) Foreleg stretching behaviour enhanced the survivor possibility of the flower mantids under predation risk.

(2) Foreleg stretching can significantly delay and reduce predator attacks, likely by intimidating the predators or confusing predatory mantids regarding the target location.

(3) Foreleg stretching can deflect predators’ attacks from the more vulnerable body trunk to the less vulnerable forelegs, thereby facilitating escape after the attack.

Characterising the types of foreleg stretching behaviours

We compared the stretching behaviour among three flower mantid species: A. basinigra, Pseudocreobotra wahlbergii, and Acromantis hesione. Type I is characterised by the alternative extension of both forelegs to opposite sides of the body axis, with each leg extending at a large angle relative to the body’s central axis (approximately 56.90°). This mode is often accompanied by the shivering of the tibia and tarsus. Type II is the simplest of the three types, involving simultaneous forward stretching of both forelegs at a much smaller angle (approximately 2.83°) to the body’s central axis, making the inner surfaces of the forelegs concealed and resembling the predatory strike behaviour during hunting. Type III involves the alternative extension and withdrawal of the forelegs in a circling motion, with the angle of stretching falling between that of type I and type II (approximately 21.99°).

Morphometrics of foreleg femurs

We selected 16 adult A. basinigra specimens (n = 8 for each sex) to measure the morphology of foreleg femurs. The length, width and thickness of the femurs were measured using a digital calliper. The right foreleg femur of each specimen was measured. Additionally, to reflect the variation in foreleg femur extension among flower mantids, we selected 93 specimens from 7 species which exhibiting 4 distinct foreleg stretching patterns (Type I, Type II, Type I+II, and Type III). The relative width (width/length) of the femur was measured for these specimens. Result revealed that at the early stage of the evolution of stretching behaviour, with the emergence of the type II behaviour, lineages exhibiting stretching behaviour showed almost no femur expansion. Greater femur expansion appeared following the evolution of the more derived stretching behaviour types, types I and III.

Frequency measurement of behaviour

To determine whether foreleg stretching behaviour occurs more frequently during moving in A. basinigra flower mantids, we selected seven 3rd instar individuals with similar moulting times. To account for the diurnal activity of mantids, video recording began at 8:00 AM and lasted for 12 hours. The experiment lasted for seven days. Result showed that foreleg stretching behaviour is frequently exhibited even when flower mantids are actively moving, a state in which they are more likely to be detected by ambushing predators. In contrast, flower mantids barely stretch their forelegs when at rest.

Speed comparison between control and treatment group

To assess whether our manipulation affected the movement speed of mantids, potentially influencing their survival under predation, we compared the mean speeds of individuals from the control (normal) group and the treatment (forelegs-disabled) group. Result showed that there is no significant difference between the two groups.

Taxon sampling and phylogenetic analyses

We utilized mitogenomes and nuclear DNA from a curated taxon set of 50 mantid species to reconstruct their phylogenetic relationships. By employing advanced mitochondrial phylogenomic workflow and ancestral state reconstruction, our results obtained the phylogenetic tree with high support value, with its topology aligning with widely accepted hypotheses of evolutionary relationships of Hymenopodidae.

Divergence time estimation and ancestral state reconstruction

To better understand the evolutionary trajectory and temporal rates of change in foreleg stretching behaviors, we conducted ancestral state reconstructions and rate estimations of character transitions using the phylogenetic relationships and foreleg stretching behavioral datasets we established for various mantodean species. Our analysis, facilitated by functions in the phytools package, suggested that the ancestral function of foreleg stretching was associated with prey capture. This function later evolved to incorporate anti-predator mechanisms within the flower mantid clade, aligning with the diversification of large-sized mantids, which are likely the primary invertebrate predators of these flower mantids.

Turning lances into shields: Flower mantids stretch their raptorial forelegs to avert and deflect predator attack

Data files

Abstract

README: Turning the lances into the shield: Flower mantids stretch raptorial forelegs to avert and deflect predator attack

Description of the data and file structure

Files and variables

File: DataS1.csv

Variables

File: DataS2.csv

Variables

File: DataS3.csv

Variables

File: DataS4.csv

Variables

File: DataS5.csv

Variables

File: DataS6.csv

Variables

File: DataS7.csv

Variables

File: DataS8.csv

Variables

File: glmm.data.xlsx

Variables:

File: Chisq.test.data.txt

File: linear.regression.data.txt

Variables:

File: DNA_Information.pdf

Information:

File: Mantidea_state_matrix.csv

Information:

File: hymenopodidae_Mantidae.csv

Codes information

Statistical.Codes

Reconstruction_of_Ancestral_States_and_rate_change_across_time

Mantidea_pruned_outgroups.tree

Species_Distribution_and_Point_Data

Version changes

Methods

Works referencing this dataset