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Mudskippers use tail thrusting to help crutching to move on mud of various wetness
Divya Ramesh, Gargi Sadalgekar, Jiangqi Tan, Chen Li
TL;DR
Amphibious fishes face poorly characterized locomotor challenges on wet flowable substrates whose strength and cohesion vary with wetness. The study tested mudskippers on controlled-wetness clay mud and found that they largely retained crutching while adding tail thrust when crutching became less effective.
Problem
How amphibious fishes adjust locomotion on wet flowable substrates of varying wetness remains relatively little studied despite changing substrate strength and stickiness.
Method
The study tested mudskippers on clay mud with controlled, variable wetness spanning the solid–fluid-transition regime and measured locomotion and mud interactions.
Results
Mud strength decreased 100-fold as wetness increased, while mudskippers predominantly retained crutching and assisted it with tail thrusting when normal crutching became less effective.
Takeaways & Limitations
The mudskipper’s crutching motor program is well adapted to native muddy substrates but inflexible, with most locomotor novelty occurring in tail use.
Takeaways & Limitations
The exact solid volume fraction of dry mud could not be calculated because its remaining water content after drying was unknown.
Abstract
from arXiv · showhide
At the water-land interface, amphibious fishes encounter wet flowable substrates made of granular solid-water mixtures, which can stay solid or flow like a fluid. As these substrates become wetter or drier, their yield strength (at which solid-fluid transition occurs) and cohesion (how sticky they are) both change, challenging locomotion. Despite substantial understanding of tetrapod locomotion on flowable substrates (mostly dry sand), we know little about how amphibious fishes cope with wet flowable substrates of various wetness. Here, we studied mudskippers on clay mud of controlled, variable wetness over the range where solid-fluid transition occurs. As mud became wetter, its strength decreased by 100-fold, leading the animal to sink deeper, with larger areas of body and fins contacting mud. By contrast, mud stuck most easily at intermediate wetness. The increased sinkage and contact and stickiness change caused more mud to stick to and pull against the animal on wetter mud. We also tested dry mud, which stuck to animal fins as its mucus dried. Despite these challenges, the mudskipper predominately used a conserved crutching gait on all except the wettest mud tested, with a modest performance reduction. When normal crutching became less effective, the animal assisted it with tail thrusting, by bending and straightening it to push downward and backward to generate additional thrust and lift, or even thrusting the tail to jump. These observations suggest that mudskipper's crutching motor program is well adapted to its native muddy substrates but inflexible, with most novelty in tail use.
1. Introduction
Amphibious fishes move across wet flowable substrates whose strength and stickiness vary with wetness, but how they adjust locomotion across such substrates remains poorly understood. This study examines mudskippers crutching on controlled-wetness clay mud.
- Substrate mechanics: Fine clay particles mixed with water generate strong cohesion, distinguishing muddy substrates from predominantly coarse-grained sandy substrates.Clay particles are smaller than 20 μm, whereas sandy particles range from approximately 20 μm to 2 cm.
- Substrate mechanics: Wet granular substrates can transition between solid-like and fluid-like behavior as applied forces exceed their yield force.Muddy substrates transition at intermediate wetness; too little or too much water produces fractured solid or viscous fluid mud.
- Locomotor challenge: Wetness changes both substrate yield strength and stickiness, so animal forces can produce either solid- or fluid-like responses and increase pulling resistance.Mud can penetrate deeply, adhere to appendages, and exert downward and backward forces; these properties vary with wetness.
- Research gap: Compared with mostly dry-sand terradynamics, amphibious-fish locomotion on wet flowable substrates of varying wetness remains relatively understudied.Earlier wet-substrate studies did not precisely control and systematically vary wetness.
- Study question: The study asks how mudskippers adjust crutching or switch locomotor modes as mud strength and stickiness change.Mudskippers use crutching and can modify it through body, tail, and fin movements on other substrates.
- Study approach: The study uses clay mud as a controllable model substrate and mudskippers as an ecologically relevant amphibious-fish model.Clay-mud yield strength and cohesion in the solid–fluid-transition regime depend on wetness, controlled through solid volume fraction.
2. Materials and Methods
The researchers prepared clay mud at controlled solid volume fractions spanning fractured-solid and solid–fluid-transition regimes, then characterized strength, stickiness, and mud adhesion with penetration, drag, and extraction tests.
- Mud preparation: Clay mud was prepared at solid volume fractions ϕ = 27%, 34%, 39%, and 42%, with dry mud representing the fractured regime.Mud was mixed with water and placed in a 1.02 m × 0.51 m × 0.16 m container filled to 0.12 m.
- Mud adhesion: Mud adhesion after sinkage was evaluated by allowing a 200 g, 2.5 cm-radius slotted disc to sink under its own weight and then extracting it.Side and oblique videos were used to measure disc sinkage and the amount of mud retained during extraction.
2.3. Animals
Five Atlantic mudskippers were housed and tested under controlled laboratory conditions, with synchronized imaging and repeated measurements of locomotion, mud interaction, and locomotor-mode use.
- Animals: The experiments tested 5 Atlantic mudskippers (Periophthalmus barbarous).Animals had mean mass 19.33 ± 4.76 g and mean body length 12.73 ± 1.65 cm.
- Animal care: Animals were housed in heated, well-lit aquaria containing brackish water and were fed dried shrimp pellets daily.Housing temperatures were 22–30 °C and water salinity was 1.01 specific gravity.
- Data collection: Webcams recorded complete daily experiments to quantify locomotor-mode transitions, tail-assisted crutching, and jumps.Mud strength was repeatedly measured at undisturbed locations to track drift throughout the multiday experiments.
- Protocol: Each animal acclimated to each mud wetness for a few minutes and rested 10–15 minutes after experimental sessions.Animals were cleaned and returned to water when drying, becoming heavily covered with mud, or jumping from the testbed.
2.5. Overview of data analyses for testing hypotheses and sample size
The analysis quantified crutching performance and three-dimensional kinematics, mud contact and sinkage, locomotor-mode transitions, tail-assisted crutching, and jumping across mud wetness conditions.
- Crutching analysis: Crutching trials were defined from sections of continuous crutching, and cycles ran from pectoral-fin touchdown to the next touchdown.Stance and swing phases were distinguished by whether the pectoral fins contacted the substrate or moved through the air.
- Crutching analysis: Performance analysis measured forward displacement per cycle Δx, average cycle speed v_c, and three-dimensional marker kinematics.Trials included at least five cycles on ϕ = 42% and dry mud, but all 1–11-cycle trials on ϕ = 27%, 34%, and 39%.
- Kinematics: Kinematic comparisons examined marker positions and event timing across mud wetness, including mid-stance, swing onset, and mid-swing.Three-dimensional reconstruction required trials with at least four cycles visible in at least three camera views.
- Mud interaction: Mud-interaction analysis measured body sinkage, body–mud and fin–mud contact, fin sinkage, upward substrate force, and mud adhesion.Fin sinkage was calculated from fin–mud contact measurements because direct measurement was difficult.
- Mode analysis: Webcam observations quantified transitions among locomotor modes, frequencies of normal and tail-assisted crutching, and the number and displacement of jumps.Only modes initiated inside the testbed were included, and jumps near boundaries were excluded from displacement analysis.
- Analysis scope: Three-dimensional kinematics were not tested on ϕ = 27% mud because mud covered the fins and most of the body, preventing reliable tracking.This condition was retained for other analyses where possible.
2.6. Crutching performance measurements
The study quantified mudskipper crutching performance, body sinkage, mud contact, and estimated substrate forces across mud conditions.
- Performance: Forward speed was calculated from displacement per crutching cycle and cycle period, then averaged across cycles for each trial.Each cycle began at pectoral-fin touchdown and ended at the next touchdown.
- Sinkage and contact: Body sinkage was measured from the difference between animal height and mud-surface height.The mud surface was identified from side-view video at mid-swing.
- Sinkage and contact: Body–mud contact length and fin–mud contact area were measured at mid-stance using side- and top-view high-speed videos.Fin contact length was estimated from the proportional relationship between contact lengths and contact areas.
- Qualitative observations: The analysis also used video observation to assess mud sticking and locomotor difficulty during trials.These observations included whether mud stuck to the animal and whether it struggled to escape.
- Force estimation: Upward substrate forces for the body and fins were estimated from mud strength, contact area, and sinkage.The calculation assumed lift was proportional to sinkage and contact area at shallow penetration depths.
- Force estimation: Fin sinkage was calculated from fin–mud contact measurements and estimated upward substrate force.Expected fin sinkage under other wetness conditions was also calculated using a constant fin contact area.
2.9. Crutching 3-D kinematics measurements
Three-dimensional crutching kinematics were reconstructed from multi-view video tracking and compared across mud wetness using cycle-level movement features and angles.
- Tracking and reconstruction: Crutching trials were analyzed for mud wetnesses ϕ = 34%, 39%, 42%, and dry mud.The study used multi-view high-speed videos to track the animal’s snout, tail, body, and pectoral fins.
- Tracking and reconstruction: DeepLabCut tracked body and fin landmarks, with a p cut-off of 0.9 used to retain high-confidence points.Tracking was visually inspected and selected frames were manually retracked when necessary.
- Tracking limitations: On mud of ϕ = 34%, fin-tip tracking occasionally shifted because the fins sank and were partly obscured.On mud of ϕ = 27%, fins and much of the body were covered, preventing the same analysis.
- Tracking and reconstruction: Three-dimensional positions were reconstructed using direct linear transformation, with coordinates rotated so +x represented trial-forward motion.Outliers were removed using median filtering, displacement thresholds, and visual inspection.
- Kinematic comparisons: The analysis calculated fore-aft, lateral, vertical, and total velocities for each tracked marker.These velocities formed the basis for comparing movement across mud wetness.
- Kinematic comparisons: Fin retraction, lateral ending, fin depression, and body vertical ending angles were calculated to quantify crutching modulation.Minimum fin retraction and depression angles during stance were compared across mud conditions.
- Kinematic comparisons: Cycle-averaged kinematics were obtained by offsetting and normalizing time and kinematic data within each crutching cycle.The study compared duty factor, mid-swing time, snout vertical displacement, and fin displacements.
2.10. Definition of other locomotor modes
The mudskipper used normal crutching alongside several alternative locomotor modes involving tail bending, tail thrusting, jumping, digging, or turning.
- Locomotor modes: Alternative modes included crutching with small or large tail bending, forward jumping, vertical jumping, digging in, and turning.These modes were documented as distinct behavioral sequences on mud.
- Tail-assisted crutching: Small tail bending added limited propulsion, producing no or partial body lift and lasting only one or two cycles.This mode resembled tail use during crutching on level dry sand and gelatin, but differed in tail motion on gelatin.
- Tail-assisted crutching: Large tail bending combined fin pushing and upward head tilt to propel part of the body upward and forward.It was sustained over multiple consecutive cycles on mud of ϕ = 27%.
- Tail-assisted crutching: On mud, large tail bending likely generated both upward substrate force and forward thrust.This differs functionally from inclined-sand tail bending, which mainly propels forward or prevents backward slipping.
- Jumping: Forward and vertical jumping used lateral tail bending followed by tail and fin pushing downward and backward.Forward jumping propelled the animal upward and forward, whereas vertical jumping propelled it vertically and included fin extension during descent.
- Other modes: Digging in involved simultaneous forward fin and slight tail motion followed by slow tail straightening as the body moved backward.The behavior allowed the animal to dig itself into the mud.
- Other modes: Turning involved rapid head and tail movement into a C-shape to change direction.The maneuver was described as similar to a C-start escape movement.
2.11. Analysis of other locomotor modes
Locomotor-mode analysis quantified behavioral transitions, relative use of tail-assisted crutching, and jumping frequency and displacement across experimental sessions.
- Transition analysis: Mode sequences were recorded from webcam videos, and transition frequencies were calculated relative to transitions from the session-start mode.A representative sequence included repeated crutching and forward jumping before finishing.
- Transition analysis: Transition diagrams retained non-self-transitions above a relative-frequency threshold of 0.089 and newly observed transitions.GraphViz was used to generate the diagrams.
- Mode frequencies: The analysis compared normal crutching, crutching with small tail bending, and crutching with large tail bending across mud wetness.Relative frequency was the average count of each mode divided by the combined average count of all three modes.
- Jumping performance: Jumping performance was quantified using vertical- and forward-jump frequency and forward-jump horizontal displacement.Jump counts were divided by session duration, and snout positions were tracked at the beginning and end of forward jumps.
2.12. Statistical tests
The study tested whether mud wetness affected crutching performance, body and fin interactions, jumping, and three-dimensional locomotor measurements using mixed-effects statistical models.
- Crutching performance: Crutching performance was evaluated using forward displacement per cycle, average forward speed, stride frequency, and cycles per trial.Trial-averaged values were pooled across individuals for each mud wetness.
- Animal–mud interaction: Sinkage and mud interaction analyses compared body sinkage, body–mud and fin–mud contact, weight support, and fin sinkage across wetness conditions.Measurements were averaged across crutching cycles and individuals for each mud wetness.
- Statistical models: Linear mixed-effects models tested mud wetness while accounting for individual variability and, where relevant, trial-to-trial variability.Individual was modeled as a random effect; crutching trial number was additionally included as a fixed effect in several analyses.
- Jumping: Jumping analyses compared jump frequency and forward jump displacement across mud wetness conditions.Jumps were averaged by individual, pooled across individuals, and analyzed with a mixed-effects model.
- Kinematics: Three-dimensional kinematics and body and fin positions were normalized, averaged across cycles or trials, and statistically compared across wetness conditions.Analyses included displacement, speed, stride frequency, body bending, fin motion, body position, and fin-placement timing.
3. Results
Mud wetness altered strength, stickiness, sinkage, and crutching performance, but mudskippers largely conserved their crutching gait. When crutching became less effective, tail bending supplied additional lift and thrust, especially on challenging mud.
- Mud properties: Mud yield strength increased monotonically as mud became drier, whereas stickiness was highest at intermediate wetness.Weaker mud at ϕ = 27% was 1–2 orders of magnitude weaker than dry and wet sand.
- Animal–mud interaction: Wetter, weaker mud caused deeper animal sinkage, larger body and fin contact, and greater downward and backward pulling from adhered mud.At ϕ = 27%, the animal contacted more mud than at ϕ = 34%.
- Crutching performance: The mudskipper predominantly used crutching across mud wetness conditions, except on the wettest mud tested.Performance reductions were associated with weakened mud, greater contact, and mud sticking.
- Crutching performance: As mud became drier from ϕ = 27% to ϕ = 42%, average forward speed increased and displacement per cycle more than doubled, then decreased slightly on dry mud.On dry mud, dried mucus caused fin sticking and increased body friction.
- Force support: On wetter, weaker mud, fin weight support decreased from 94% of average body weight at ϕ = 42% to about two-thirds at ϕ = 27%.Body-supported weight correspondingly increased from 3% to one-third of average body weight.
- Crutching kinematics: Crutching kinematics remained mostly conserved across mud wetness, with body lift during early stance and forward propulsion with little lateral motion.This pattern was similar to crutching on solid ground.
- Tail-assisted locomotion: When normal crutching became less effective, tail bending assisted crutching by generating upward lift and forward thrust, and tail thrusting also produced jumps.Large tail bending dominated attempts on ϕ = 27%, while small and large bending were less frequent on ϕ = 34%.
4. Discussion
Mud is weaker and stickier than sand across changing wetness, creating substantial locomotor challenges. Mudskippers largely retain crutching but adjust support and rely on tail thrusting and other modes when crutching becomes less effective.
- Greater challenges on mud: Mud stickiness depended on both wetness and the amount of mud attached, with intermediate wetness maximizing sticking and dry mud producing ice-like adhesion.As mud became wetter, increased contact and stickiness caused more mud to adhere and pull against the animal.
- Responses to changing mud properties: Wetter, weaker mud caused deeper sinkage and larger body–mud and fin–mud contact areas.The mudskipper reduced stride frequency, completed fewer consecutive cycles, shifted support toward its fins, and increased fin contact on the weakest mud.
- Greater challenges on mud: Mud became up to 100-fold weaker while also producing downward and backward pulling through adhesion.Wetter mud reduced yield strength by up to two orders of magnitude; mud’s resistance during extraction further increases locomotor costs.
- Tail-assisted locomotion: On the weakest mud at ϕ = 27%, the mudskipper stopped normal crutching after one cycle and used tail assistance or jumping.This response occurred after stepping into previously disturbed mud, where other animals and robots can lose forward progress.
- Control strategy: Crutching appears to be a stereotypical, mostly inflexible gait template, whereas the tail is the body region controlled most flexibly.The trunk and fin motor patterns remained comparatively conserved while tail use expanded as mud became more challenging.
- Tail-assisted locomotion: When crutching became less effective, the mudskipper used small or large tail bending, forward or vertical jumping, and other locomotor transitions.These strategies primarily used tail thrusting to generate upward lift and forward thrust, especially on challenging mud.
Funding
The study was funded by a Burroughs Wellcome Fund Career Award at the Scientific Interface and a Johns Hopkins University Bridge Grant.
- Funding came from a Burroughs Wellcome Fund Career Award at the Scientific Interface and a Johns Hopkins University Bridge Grant.
Supplementary figures
Supplementary figures document crutching performance, displacement, velocity, timing, and body and fin kinematics across mud wetness conditions.
- Supplementary figures compare crutching performance and forward displacement across cycles and mud wetness conditions.Figure S2 includes forward displacement per cycle as a function of cycle number and average slopes across five wetness levels.
- Figure S2 notes that the average slope for ϕ = 27% is not statistically meaningful because it comes from one experimental day.
- Supplementary kinematic figures quantify body and fin displacements, velocities, phase timing, and stance-related motion over crutching cycles.Measurements include forward, lateral, and vertical motion for the body and both pectoral fins.
- Supplementary figures examine conserved three-dimensional body and pectoral-fin motions across mud wetness.Figure S5 emphasizes relatively conserved kinematics, limited body bending, and fin rotations during normal crutching.
- The supplementary analyses define tracked markers and angular measures for body bending, fin retraction, and fin depression.Body angles α1–4 and β1–4 and fin angles αL,R and βL,R are evaluated over the cycle.
Supplementary Movies
Supplementary movies show passive sinking and mudskipper locomotion, including normal crutching, tail-assisted crutching, jumping, digging, and turning.
- Movie 1 shows passive weight sinking tests on mud of different wetness.
- Movie 2 shows normal crutching, small tail bending, and large tail bending on mud.
- Movie 3 shows forward and vertical jumping, digging in, and turning.