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Animal Locomotion in Different MediumsThe Adaptations of Wetland Organisms

Abdul Jamil Urfi

KeywordsWetlands, animal locomotion,medium, terrestrial, aquatic,mudskipper.

Abdul Jamil Urfi isAssociate Professor atDepartment of Environ-mental Studies, Universityof Delhi. His previousarticles in Resonance

include Breeding Ecologyof Birds. Why do SomeSpecies Nest Singly WhileOthers are Colonial ?

(July 2003) and Grapplingwith ‘Natural Selection’ –Experiences of a Teacher

(May 2013).

Wetlands are repositories of unique biodiversity. Wetlandorganisms are well adapted to their habitat, lying at theinterface of aquatic and terrestrial environments. In order tounderstand their adaptations in a better way, it is essential tograsp the basic properties of the medium in which variousorganisms live. This is attempted here by first examining theproperties of the two contrasting environments, terrestrialand aquatic. We focus primarily on locomotion, touchingupon related life processes like respiration, body size andmaintaining body balance by employing basic principles ofbiology and physics.

To say that all living organisms live in a ‘medium’ is to state theobvious. We usually have a fair idea as to what the term means.Fishes, plankton, squids, sea turtles, whales, etc., all aquaticcreatures, live in water, while tigers, bears, elephants and lizardslive on the ground and are terrestrial. All birds belong to the lattercategory, though at various phases of their life some taxa maydepend upon aquatic resources for food or nesting and hence aresomewhat erroneously labelled as ‘aquatic birds’. Amphibians(from Amphibios; amphi meaning ‘of both kinds’ and biosmean-ing ‘life’), as the name suggests, are a group of vertebrates whichinhabit two worlds. Their initial phase, when the organism comesinto being and lives as a larval tadpole is spent in the wateryenvironment. The succeeding adult phase is usually spent in theterrestrial environment as a frog, hopping around on the groundand catching insects and other grub for a living. However, at thetime of reproduction, the calling from the aquatic world is verystrong indeed and so that is where it returns to for spawning. Likethe amphibians, wetland organisms too live in both mediums,viz., water and air but with a crucial difference. In their case, the

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two mediums exist side by side, unlike the amphibians, which arewholly aquatic in one phase and terrestrial in the other.

Life in Contrasting Environments: Aquatic and Terres-trial Habitats

Before we examine the adaptations of wetland organisms, it willbe useful to review the physical properties of the two contrastingmediums and examine how the constraints imposed by the envi-ronment have a bearing on vital life processes. We shall focus onlocomotion, which is a significant trait of all living organisms(see Box 1). Keeping the exceptions aside, in this article, weexamine only self-powered animal locomotion. To set the stagefor the discussion to follow, the relevant physico-chemical char-acteristics of aquatic and terrestrial environments are summarized inTable 1. In a terrestrial habitat, the all-pervading medium is ofcourse air, which is a mixture of gases, chiefly nitrogen, oxygen,carbon-dioxide, etc. In an aquatic environment, which could bestill (lentic) or flowing (lotic), saline or freshwater, dependingupon the salt concentration in it, the medium is water.

Countering Drag

The resistance offered by the medium to a moving body variesconsiderably in rare and dense fluids. For instance, a personwalking on a road does not encounter much resistance and so shecan move about more or less effortlessly from point A to B in ahorizontal plane. But imagine if she was in a room filled with adense fluid, say glycerine or honey (and let us also assume forsimplicity that breathing was not an issue in this case). Here, shewould have great difficulty in walking across the room becausethe dense medium would offer resistance. Let us examine thisfurther.

Principally, two forces, perpendicular to each other, are acting onall bodies whether they are inside water or on the ground. One isthe gravitational pull and second, as they move, the resistanceoffered by the medium. In the case of fishes, which are typical

Like the amphibians,wetland organisms

too live in bothmediums, viz., water

and air but with acrucial difference. Intheir case, the two

mediums exist side byside, unlike the

amphibians, whichare wholly aquatic in

one phase andterrestrial in the other.

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Box 1. Mobility in Different Life Forms

At different phases of their life cycle both animals and plants are highly mobile but their modes of locomotion/transport differ. Plants are rooted and immobile as adults but as seeds they are usually highly mobile, havingadaptations for dispersal through air and water (Fig. A & B) with the assistance of various structures and tissuemodifications (wings, feathers, husk etc). In the case of animals the situation is reverse in that their young arefairly immobile or localized (eggs or nestlings, cubs in a den etc) but as adults they are highly mobile. Since,animals cannot obtain all their requirements by being at the same spot, as plants do by extending their roots inthe direction of moisture and nutrients, animals forage actively by travelling to areas where food is available.However, there is a huge diversity of locomotory modes. Sometimes, animals may need to move quickly whileforaging (sit and wait predators) and at other times may chase their prey over long distances (pursuitpredators). Also, many a times, they may need to flee from predators or other forms of danger in which theirmovements are akin to sprinting action. For each of these tasks the laws of mechanics dictate the amounts ofeffort required, which of course varies in different environments.

While most animals are capable ofself powered locomotion there arealso several examples from theanimal kingdom where the organ-isms drift passively. For example,the medusa of Coelenterates have asail like structure which assists inwind driven transport (Figure C).There are also examples of animalsmoving at the interface of waterand air, as in the case of Penguin,Flying Fish, Dolphin etc (Fig. Fand G). This strategy, by alternat-ing in twomediums, one very denseand the other rare, is believed toconsiderably reduce the energeticcosts of locomotion by reducingdrag forces. Plankton, usually mi-croscopic invertebrates, have nopowers of locomotion of their ownand drift along ocean currents (Fig-ure D and E). They contrast withnekton (fishes) which are capableof powered locomotion (Figure H).

Figure. A. Airborne seeds. B. Coconut with husk around awoody case which helps in floating. C. Medusa with the sailorgan. D. Daphnia (zooplankton). E. Diatom (phytoplankton).F. Dolphin. G. Flying Fish. H. Shark.

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aquatic organisms, both these forces are in operation, but becauseof the buoyancy of the medium the gravitational pull is consider-ably less in magnitude. However, as far as the forward movementis concerned, the drag forces tend to act upon them immediatelywhen they move. Simple mechanics tells us that in such a situa-tion, large amounts of force would be required to bring a body inmotion from a position of rest, but once it is in motion (cruising)much less force would be required to sustain that movement.(More or less the same idea, based on Newton’s laws of motion,holds for the gear shifts in a car.) The streamlined shape of fishesand the mucous coating over their bodies are all adaptations forreducing drag forces.

Table 1. Some relevant physico-chemical characteristics of terrestrial and aquatic environments and themanner in which they have a bearing on life processes.

Medium Aquatic Terrestrial(freshwater or saline water) (air/gases)

Medium Properties

Density/viscosity High Low

Dissolved oxygen Low (0.5%) High (20%)

Force of gravityexperienced by theorganism Low High

Respiratory adaptations Structures (gills, skin, etc) Structures (lungs) toto absorb oxygen dissolved absorb Oxygen in airin water. Supplementingwith cutaneous respiration.

Individual growth and Can grow quite large Usually small/mediumbody size

Forward movement Energetically expensive Energetically cheaper

Locomotory adaptations Body shape streamlined Greater need for organsto minimize drag of balance maintenance

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Countering Gravity

The situation in terrestrial environments is reverse where forwardmovement is not so expensive, in energetic terms, as is counter-acting the forces of gravity. This means, as far as terrestrialanimals are concerned, beyond a point it would become veryexpensive to grow bigger in size as it would require a strongskeleton and muscles to bear that much additional body weight.Organisms living in water are relatively free of such restrictions.Extant terrestrial mammals such as elephants, large as they are,cannot match the body size of aquatic mammals such as whales.While the male African elephant (Loxodonta africana).is re-corded to weigh about 6 tonnes [1], it is nearly 28 times lighterthan the blue whale (Balaenoptera musculus), which can weighup to 170 tonnes [2]. The possibility of acquiring mass is there-fore immense in the aquatic environment. This, however, doesnot preclude the possibility of terrestrial animals being large, butthen some unique factors are responsible for their sizes. A case inpoint is the giant tortoise on islands, where some specific factors– ‘island gigantism’ [3], tend to operate.

As we have noted above, the largest animals like the whales areocean dwellers. Their body mass is enormous but their skeletalframe is only strong enough to withstand the forces operating inan environment where buoyancy is high. If such huge creaturescome out of water, as it happens sometimes, i.e., when they getstranded on the beach during the turning of the tide, then, as theirskeletal system snaps, they can be literally crushed under theirown weight. From time to time, we keep hearing of cases ofbeaching of whales on the Indian coast [4]. Death in such situa-tions can also happen due to asphyxiation or when high tidecovers the blowhole.

The influence of physical constraints imposed by the environ-ment are ubiquitous and plants are equally affected. Gravity isstill the key factor and adaptations for withstanding forces ofgravity, such as a strong structural tissue is warranted. Therefore,in comparison to their aquatic counterparts, terrestrial plants,

As far as terrestrialanimals areconcerned, beyond apoint it would becomevery expensive togrow bigger in size asit would require astrong skeleton andmuscles to bear thatmuch additional bodyweight. Organismsliving in water arerelatively free of suchrestrictions.

If huge creatureslike whales comeout of water, as ithappenssometimes,i.e., when they getstranded on thebeach during theturning of the tide,then, as theirskeletal systemsnaps, they can beliterally crushedunder their ownweight.

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especially those species which grow quite large in height, investheavily in structural tissue (xylem). Yet, due to the buoyancyafforded by the medium, aquatic plants have little need to investin woody tissue. Anyone who has maintained an aquarium withwater plants in it would have noticed how plants like Vallisneriaand others, which look beautiful and ‘full of shape’ under water,collapse and loose their form when water is drained from thevessel in which they are displayed.

Adaptations at the Physiological Level

Since animals require moving about in different ways, viz.,cruising, sprinting, their skeletal muscle tissue – responsible forvoluntary movements – is very heterogeneous. Principally, it iscomposed of slow, contracting ‘red’ fibres (because of theirhigher vascularisation and consequently their higher myoglobincontent they tend to have a red colour) and fast contracting‘white’ fibres (poor vascularisation and consequently lower myo-globin content). While the former uses the pathway of aerobicmetabolism for the production of ATP (energy packets in thecells), the latter uses anaerobic glycolysis (Table 2). Aerobicpathways, represented by the TCA cycle or the Krebs’s cycle,first convert glucose into pyruvate by glycolysis and then com-pletely oxidize it to CO2 and H2O using molecular oxygen. Inanaerobic glycolysis, the muscles use glycogen to generate ATPwith lactate as the end product. In the event of a sprint, lactate

Table 2.Thedifferencesbetween the slow andfast muscle fibres.

Parameters Slow fibres Fast fibres

Colour Red WhiteMetabolism Oxidative Anaerobic GlycolysisPrecursor Glucose/Fats GlycogenEnd Products H2O, CO2 LactateFibre diameter Small LargePower generation Small LargeSustainability Long term Short termVascularisation High Low

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tends to accumulate in high concentrations and is slowly convertedby the liver into glucose during a ‘rest’ or ‘recovery’ phase. Theexcess oxygen consumed in the recovery period represents therepayment of the oxygen debt [5].

The Musculature of Fishes

Fishes, moving in water encounter drag forces, which can be ofconsiderable magnitude. If sudden movement is required to catchprey or escape predators in a viscous medium, it is only possibleby the contraction of fast, white muscle fibres, which rely onanaerobic glycolysis pathways. Therefore, it is not surprising thatfishes have huge amounts of ‘white’ fibres in their myotomalmass which is rich in glycogen and can be rapidly mobilized byanaerobic pathways for ATP generation (Figure 1). Because ofits large size, the myotomal mass cannot have a high densitycapillary network. But the slow contracting red fibres which relyupon oxidative pathway and yield much more ATP per mole ofsubstrate, require a network of capillaries. Therefore, in mostfishes these two types of fibres, each with different properties, are

Figure 1. Transverse section of common carp(Cyprinus carpio) myotomal muscle. The bulk of themyotomal mass consists of fast contracting whitefibres while the red fibres are localized in the form ofa cone at the region of the lateral line. Thephotomicrograph’s on the left shows the red musclecone with the lateral line running through it. The uppersection has been stained for the oxidative enzymeSuccinic Dehydrogenase (SDH). Arrow indicates redsmall diameter fibres (R). The intermediate or pinkfibres are marked P while the anaerobic white or fastfibres are marked W. Note different levels of SDHactivity in different types of fibres. The lower sectionshows the activity of the enzyme myofibrillar ATPase(m-ATPase) which shows the reverse activity patternin the red fibres compared to SDH. While these fibresstain weakly, the pink and white fibres stain well for m-ATPase. Source of the photomicrographs [6].

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segregated. The slow contracting but highly vascularised ‘red’fibres are stacked in the form of a cone in a transverse section, atthe region of the lateral line while the fast contracting white fibrestend to occupy the bulk of the myotomal mass [6]. This is ofcourse a generalization in that many fishes have red fibres embed-ded in their myotomal mass. Also, there is usually a third fibrecategory, known as ‘pink’ fibres which are intermediate betweenthe two extremes, red and white fibres, in terms of their character-istics.

Inhabiting Two Worlds: Wetland Organisms

Wetland [7] organisms live in an environment which is neitherfully aquatic nor completely terrestrial, but a mixture of the two.TheRamsar Convention defines wetland as, “Areas of marsh, fen,peatland or water, whether natural or artificial, permanent ortemporary, with water that is static or flowing, fresh, brackish orsalt, including areas of marine water the depth of which at lowtide does not exceed six metres”. Note that this definition touchesupon all aspects of wetlands and covers a variety of water-loggedareas or land areas that are wet. Besides being shallow there isalso an element of ‘impermanence’ of water in a wetland in thatthe water level fluctuations can vary both seasonally (say beforeand after the monsoon rains) and diurnally (in coastal areas due tothe tides). So there is a submerged phase when a wetland is not awetland and a phase at low tide, when the shore is exposed and awetland comes into being.

The Ramsar definition also clarifies upon the land part of wet-land, which here means the substrate. This can be anything, viz.,sand, coral, rocks, and the resultant wetland could be marsh, fen,peat land, etc. The biota of wetlands is quite diverse as theanimals and plants from both the terrestrial and aquatic worldsinhabit them, due to an edge-effect. Fishes, inhabitants of thewatery world, have several adaptations for an aquatic existenceand some have already been discussed above. The plants tooposses interesting adaptations, a good example of which is man-

Wetland organismslive in an environmentwhich is neither fully

aquatic nor completelyterrestrial, but a

mixture of the two.

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groves [8]. Birds chiefly belonging to taxa Charadriiformes (wad-ers) and Anatidae (waterfowl) are generally an important compo-nent of wetland biota.

The Mudskipper:Unique Adaptations for a WetlandExistence

Wetland organisms inhabit a rapidly changing environment whichis aquatic at one moment and terrestrial at another. One type offish which serves to illustrate very well the unique adaptations ofwetland organisms is the mudskipper (Figure 2). These creatures(Boleophthalmus, Periophthalmus, Periophthalmodon etc) aredenizens of the intertidal zone and are truly unique creatures.Although taxonomically they are all fishes (family Gobiidae)they behave like ‘semi-terrestrial’ organisms, which suits theirlifestyle in the habitat lying at the junction of land and the sea [9,10]. In this wet terrestrial environment, mudskippers defendterritories against rivals and obtain their food by catching insectsor invertebrates flying about in the air. Like fishes they have gillsfor respiration but these are very rudimentary and the bulk ofoxygen uptake occurs through cutaneous respiration (skin isaccordingly slimy and wet to facilitate gas exchange processes.)Infact, they can literally drown if submerged in water for a long

Figure 2.Mudskipper in theirintertidal habitat. Note themodified pectoral fins whichhold the body in a stable po-sition. The eyes are on top ofthe head, keeping an eye onthe happenings in the terres-trial world. The tail and lowerparts of the body are alwaysin contact with water, facilitat-ing cutaneous respiration.Source [11].

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time. Yet, in their intertidal habitat, mudskippers are seldom awayfrom small pools of water which form in the sand as the tiderecedes. Their tail which is heavily vascularised to facilitate gasexchange is always dipped in water.

An interesting feature of this fish is that its eyes are placed on thetop of the head (Figure 2), instead of sideways as is the case withmost fishes. This is largely because in the terrestrial-aquaticinterface, the danger is likely to come from above. Interestingly,while the eyes are well adapted for aerial vision, they functionpoorly under water. The eyes are placed in cups formed from skinfolds which are filled with water. Since the eyes can becomeeasily dehydrated by exposure to the air, they can be retracted intothis cup and moistened as and when required.

To maintain balance and move on land, the animal requiresstructures similar to limbs. A lot of fishes have modified pectoralfins which serve the function of rudimentary limbs, particularlyDipnoi or the lungfishes. But in Dipnoans, the modified pectoralfins are bereft of an internal skeleton. Without bones or cartilage,the fins are not strong enough to support the body weight,especially when the animal is on land. We know from the evolu-tionary history of vertebrates [12,13] that the first attempt in thisdirection, i.e., evolution of vertebrates from water to land, isexemplified by Coelocanths (Latimeria), which have a rudimen-tary internal skeleton in the pectoral fins (hence the name ‘lobefins’), besides several other structural adaptations. In the case ofmudskipper, being a true fish, it is too early in its phylogeny forthe pectoral fins to have evolved substantially to support the bodyweight or even enable the animal to walk. At the most they areuseful for maintaining position on land and much of the move-ment happens by jerks of the body musculature, jumping off fromone spot and landing a few feet away.

Conclusion

By employing simple principles of biology and physics we canappreciate how the medium exerts a strong influence on life

An interesting featureof this fish is that itseyes are placed onthe top of the head,instead of sidewaysas is the case with

most fishes.

Tomaintainbalance andmoveon land, the animalrequires structuressimilar to limbs.

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forms, resulting in interesting adaptations for locomotion, bodysize, respiration, balance etc. Since wetlands have properties ofboth the aquatic and terrestrial habitats, several life processes ofwetland organisms display adaptations to an existence in rapidlychanging habitats, having elements of both the two worlds.Mudskippers, being true fish, cannot be on the line which led tothe evolution of terrestrial vertebrates (since no extant taxa,including the Dipnoans, can claim that spot [13]). However, likeseveral other fishes which have structures for survival on land(say ‘accessory breathing’ organs) mudskippers provide for agood case study of adaptations for survival in coastal wetlands.

Acknowledgments

I thank the University of Delhi for providing funds under itsschemes to support faculty research and DST-Purse grants. Thisarticle is partly based on my experiences of teaching aboutsurvival adaptations for wetland organisms in the MA/MSc Envi-ronmental Studies course at the University of Delhi and I thankthe several students who attended my course and asked intelligentquestions or gave their valuable feedback.

Suggested Reading

[1] African bush elephant,https://en.wikipedia.org/wiki/African_bush_elephant

[2] Blue whale, https://en.wikipedia.org/wiki/Blue_whale[3] A L Jaffe, G L Slater and M E Alfaro, The evolution of island gigantism

and body size variation in tortoises and turtles, Biology Letters, Vol.7,No.4, pp.558–561, 2011. doi:10.1098/rsbl.2010.1084. PMID 21270022.

[4] J Mazoomdar, Express Explained: Why beaching of whales still bafflesscience, Indian Express, January 14, 2016. http://indianexpress.com/article/explained/why-beaching-of-whales-still-baffles-science/

[5] D L Nelson and M M Cox, Lehninger Principles of Biochemistry, 6thEdition, Macmillan, 2013.

[6] C LTalesara and A J Urfi, A histophysiological study of muscle differ-entiation and growth in the Common Carp Cyprinus carpio Var, Com-munis, J. Fish Biology, Vol.31, pp.45–54, 1987.

[7] See Resonance, Vol.18, No.8, 2013.[8] P B Tomlinson, The Botany of Mangroves (Cambridge Tropical Biology

Series), Cambridge University Press, 1995.

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[9] J K De and N C Nandi, A note on the locomotory behaviour of themudskipper Boleophthalmus boddarti, Indian Journal of Fisheries ,Vol.31, pp.407–409. 1984.

[10] C M Pace and A C Gibb, Mudskipper pectoral fin kinematics inaquatic and terrestrial environments, Journal of ExperimentalBiology, Vol.212, pp.2279–2286, 2009, doi: 10.1242/jeb.029041

[11] A group of mudskipper’s on land, picture (unidentifiedPeriopthalmus) from ‘Mudskipper Army in Borneo’ by Jon Robson,19 February 2009. Wikimedia Commons.h t t p s : / / c ommo ns .wi kimed i a . o r g /wi k i / F i l e :A_ g r o up_ o f _mudskipper_on_land.jpg#metadata

[12] E H Colbert, Evolution of the Vertebrates: A History of the BackbonedAnimals, Wiley-Blackwell; 5th Edition, 5 October 2001.

[13] U Kutschera and J M Elliott, Do mudskippers and lungfisheselucidate the early evolution of four-limbed vertebrates? Evolu-tion: Education and Outreach, Vol.6, No.8, 2013 doi:10.1186/1936-6434-6-8.

[14] Q Bone and R H Moore, Biology of Fishes, 3rd Edition, Taylor &Francis, London, 2007.

[15] Ramsar, http://www.ramsar.org/[16] A J Urfi, Teaching about wetlands, NewsEE, Centre for Environmental

Education.

Address for CorrespondenceA J Urfi

Associate ProfessorDepartment of

Environmental StudiesUniversity of Delhi

New Delhi 110007, India.Email: ajurfi@rediffmail.com