University of Groningen Burrow Ventilation in the Tube-Dwelling

University of Groningen Burrow ventilation in the tube-dwelling shrimp Callianassa subterranea (Decapoda Thalassinidea) - I. Morphology and motion of the pleopods, uropods and telson Stamhuis, E. J.; Videler, J. J. Published in: Journal of Experimental Biology IMPORTANT NOTE: You are advised to consult the publisher's version (publisher's PDF) if you wish to cite from it. Please check the document version below. Document Version Publisher's PDF, also known as Version of record Publication date: 1998 Link to publication in University of Groningen/UMCG research database Citation for published version (APA): Stamhuis, E. J., & Videler, J. J. (1998). Burrow ventilation in the tube-dwelling shrimp Callianassa subterranea (Decapoda Thalassinidea) - I. Morphology and motion of the pleopods, uropods and telson. Journal of Experimental Biology, 201(14), 2151-2158. Copyright Other than for strictly personal use, it is not permitted to download or to forward/distribute the text or part of it without the consent of the author(s) and/or copyright holder(s), unless the work is under an open content license (like Creative Commons). Take-down policy If you believe that this document breaches copyright please contact us providing details, and we will remove access to the work immediately and investigate your claim. Downloaded from the University of Groningen/UMCG research database (Pure): http://www.rug.nl/research/portal. For technical reasons the number of authors shown on this cover page is limited to 10 maximum. Download date: 25-09-2021 The Journal of Experimental Biology 201, 2151–2158 (1998) 2151 Printed in Great Britain © The Company of Biologists Limited 1998 JEB1470 BURROW VENTILATION IN THE TUBE-DWELLING SHRIMP CALLIANASSA SUBTERRANEA (DECAPODA: THALASSINIDEA) I. MORPHOLOGY AND MOTION OF THE PLEOPODS, UROPODS AND TELSON EIZE J. STAMHUIS* AND JOHN J. VIDELER Department of Marine Biology, University of Groningen, PO Box 14, 9750 AA Haren, the Netherlands *e-mail: [email protected] Accepted 5 May; published on WWW 25 June 1998 Summary The morphology of the pleopods, uropods and telson of A shrimp, wandering through the burrow or resting, the tube-dwelling shrimp Callianassa subterranea have holds its pleopods against the abdomen with the exopodites been studied using dissection microscopy and scanning and their setal fringes retracted medially. The uropods are electron microscopy. The kinematics of these appendages folded medially as well, probably to reduce the shrimp’s were examined by motion analysis of macro-video drag. During ventilation, the uropods are extended against recordings of ventilating shrimps in transparent artificial the tube wall, leaving only a small opening for flow ventral burrows. The pleopods show the usual crustacean from the telson, and the pleopods beat at a frequency of biramous anatomy, but all segments are rostro-caudally approximately 1 Hz (0.9±0.2 Hz). Fourier analysis of flattened. The protopodite bears a triangular medially pleopod kinematics showed that the motion pattern of the oriented endopodite and a scoop-shaped exopodite. The first flow-generating pleopod pair (PP1) consisted mainly contralateral endopodites are linked by the appendix of the first harmonic (75 %) and to a lesser extent of the interna, ensuring a perfect phase relationship between third harmonic (20 %), resulting in almost perfect contralateral pleopods. The outer rims of the exopodites sinusoidal motion. The motion patterns of PP2 and PP3 are fringed with long fern-leaf-like plumose setae bearing could be modelled by assigning pure sinusoids with a 120 ° flattened setules. These setae have very mobile joints and phase shift and a rostro-caudal ranking to the three pairs can be turned caudally. The slits between contralateral of pleopods. endopodites have rims of leaf-like setae as well. Setae of the same leaf-like type fringe the uropods, but these are non- Key words: burrow ventilation, pleopod, uropod, telson, motile. The telson has a narrow fringe of leaf-like setae, morphology, motion analysis, tube-dwelling shrimp, Callianassa locally interrupted by long mechanoreceptory setae. subterranea, ventilation posture, metachrony, kinematics. Introduction The abdomen of decapod crustaceans consists of six Barlow, 1980; Barlow and Sleigh, 1980). Metachronal wave segments and the telson. The anterior five segments each bear patterns can be ad-locomotory (=antiplectic) or contra- a pair of pleopods, and the sixth segment bears one pair of locomotory (=symplectic), depending upon whether uropods. The uropods and the telson form the tail-fan. Pleopod coordination is in the direction of swimming or in the opposite morphology is rather variable among the decapods and is direction, respectively (Sleigh and Barlow, 1980). Depending related to their main function, which is commonly propulsion on inter-limb distance and phase shift, single pleopods in a or reproduction (Bell, 1905). Pleopods used in propulsion metachronal system may perform a complete and undisturbed usually resemble a slightly curved flat plate, a shape that is beat cycle or may move together with the pleopod of an optimal for paddling (Alexander, 1968; Vogel, 1994). The adjacent segment during part of the cycle, showing sudden pleopod area is often increased during the effective stroke by advances and delays compared with an undisturbed beat cycle spreading the rims of the setae as well as extending the podites, (Alexander, 1988; Lochhead, 1961). and the area is decreased during the recovery stroke by folding The thalassinids use pleopod beating to generate a flow of the setae and drawing the podites together (Lochhead, 1977). water through their burrow (Dworschak, 1981). The burrow In swimming crustaceans, pleopods usually show can be ventilated for filter-feeding purposes, as in most metachronal beat patterns, which are assumed to be Upogebiae, or mainly for respiratory purposes, as in most energetically advantageous (Lochhead, 1961; Sleigh and Callianassidae (Atkinson and Taylor, 1988). Burrow 2152 E. J. STAMHUIS AND J. J. VIDELER ventilation is assumed to be energetically expensive (Atkinson These motion patterns revealed sudden phase advances or and Taylor, 1988) and is always performed periodically (Farley delays in the metachronal waves due to interactions between and Case, 1968; Torres et al.; 1977; Felder, 1979; Dworschak, adjacent pleopod pairs. Fourier analysis was used to study the 1981; Mukai and Koike, 1984; Scott et al. 1988). Ventilation harmonic components of the motion patterns. The resulting bouts tend to be shorter in Callianassidae than in Upogebiae phase relationships and harmonic components were used to (Dworschak, 1981; Mukai and Koike, 1984; Forster and Graf, model the motion patterns of the pleopod tips. The changing 1995; Stamhuis et al. 1996), probably because of differences postures of the uropods and telson during ventilation were in feeding strategy. The mechanism of burrow ventilation in drawn from the video images. thalassinids has been little studied quantitatively, and very little is known about the morphology of the pleopods and their kinematics during burrow ventilation. The aim of the present Results study is to describe the morphology, postures and motion Macro- and micro-morphology patterns of the pleopods, uropods and telson of the thalassinid The third, fourth and fifth abdominal segments each carry shrimp Callianassa subterranea during burrow ventilation. one pair of pleopods used to generate the ventilation current. Each pleopod consists of a rostro-caudally flattened protopodite with two rami: a scoop-shaped curved exopodite Materials and methods and a flat medially oriented endopodite (Fig. 1). Callianassa subterranea (Montagu) of approximately The left and right endopodites of each segment are 40 mm total length were collected from box core sediment interlocked at their medial rims by a short appendage called samples at the Oyster Grounds and at the Frisian Front, central the ‘accessory ramus’ (Bell, 1905) or ‘appendix interna’ North Sea, at approximately 53°45′N and 4°30′E. Sampling (Lemaitre and de Almeida Rodrigues, 1991) (Figs 1, 2). The trips were made in October 1989 and May 1990 on the Dutch exopodites are able to spread out laterally over a small angle. research vessel ‘Aurelia’. For morphological studies, The lateral and ventral rims of the exopodites as well as the approximately 20 specimens were killed on board using a 12 % lateral and medial rims of the endopodites bear a row of solution of formaldehyde in sea water and preserved in a 4 % densely implanted segmented setae (Fig. 3). The setae have solution of formaldehyde in sea water. Other animals were infra-cuticular joints, allowing medio-lateral and dorso-ventral stored separately in small containers and transported to the motions. They are of the plumose ‘leaf’ type with flattened laboratory alive. For details of collection procedures, transport setules. The rims of the exopodites and ventral parts of the and storage conditions, see Stamhuis et al. (1996). endopodites contain a pattern of branching membranous Macro- and micro-morphological studies were made of the abdominal appendages involved in burrow ventilation. A dissection microscope equipped with a camera lucida was used for the macro-morphological studies. Photographs of micro- A3 structures were taken using scanning electron microscopy after preparation of the appendages involving critical-point drying and sputter coating. The abdominal appendages are classified according to Biffar (1971). For the setae,

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