Plasticity in the purple sea urchin (Strongylocentrotus purpuratus): Tube feet regeneration and adhesive performance

https://doi.org/10.1016/j.jembe.2020.151381Get rights and content

Highlights

  • Sea urchins are highly plastic in their tube feet morphology

  • Substrate lithology appears to influence the plasticity of tube feet

  • Regenerating tube feet do not recover pre-amputation attributes when kept ex situ

  • Disc area decrease in ex-situ conditions, but tenacity and length remain constant

Abstract

Sea urchins are key members of hydrodynamically intense habitats, such as open coast intertidal and shallow reefs. Secure attachment to the substrata, by means of tube feet and spines, is essential for survival. Previous studies suggest that environmental variables (i.e. hydrodynamics, substrate) can influence the morphology and adhesive performance of tube feet. Catastrophic failure of tube feet occurs often due to strong hydrodynamic forces. The time and ability of amputated tube feet to return to pre-amputation adhesive performance, and the interaction with environmental factors are unknown. To assess the dynamics of adhesive performance and regeneration of tube feet, we 1) evaluated phenotypic plasticity of disc surface area of two urchin populations inhabiting sites with different lithologies (field - in-situ conditions) and, 2) assessed regeneration of their functionality (tube foot length, time of disc first appearance, disc surface area, and tenacity) after amputation (laboratory - ex-situ conditions). Results showed that in the field, tube feet are plastic in their phenotype: sea urchins from the two sites differed in their disc surface area. Plasticity was also observed in the laboratory, where urchins regenerate tube feet that are shorter in length and have smaller discs compared to pre-amputation measurements. Thus, sea urchin tube feet recovering from amputation events in the intertidal may differ in their initial morphology and in the recovery period after amputation. Moreover, tube feet that were never amputated also decreased their disc area, suggesting that plasticity occurs on tube feet of urchins maintained in laboratory conditions. In shallow temperate reef systems, urchins are ecosystem engineers that affect the abundance and distribution of many other organisms. The plastic nature of morphological and adhesive abilities of sea urchin tube feet influences their ability to survive and dominate wave-battered habitats.

Introduction

Organisms with the same genotype can express a variety of phenotypes depending on environmental conditions. This broad definition of phenotypic plasticity includes changes in morphology, behavior, physiology, growth, life history and demography, and occurs in response to biotic and abiotic aspects of their environments (DeWitt and Scheiner, 2004; Pigliucci, 2001). Phenotypic plasticity allows organisms to respond to environmental shifts with, mostly beneficial (but see: DeWitt et al., 1998), phenotypic changes and influences the ecology and evolution of species (Pigliucci, 2001). Ecologically, phenotypic plasticity is especially important when the environmental change happens over relatively short periods of time or is patchy in space, and when different phenotypes differ markedly in performance under different conditions.

Marine organisms provide important examples of phenotypic plasticity (reviewed in McAlister and Miner, 2017; Miner et al., 2005; Padilla and Savedo, 2013). Sea urchins, in particular, are well known for their morphological, physiological and behavioral plasticity (i.e. Adams et al., 2011; Crook and Davoren, 2016; Dumont et al., 2007; Ebert, 1996; Haag et al., 2016; Harding and Scheibling, 2015; Russell, 1998; Urriago et al., 2011). Benthic (juveniles, adults) and pelagic (larvae) stages show rapid morphological response of hard structures to food availability (i.e. Adams et al., 2011), substrate complexity and lithology (Hernández and Russell, 2010; Russell et al., 2018), and the presence of predators (Selden et al., 2009). Studies of plasticity in sea urchin soft structures, however, have been focused on ciliated bands associated with feeding and swimming in larvae (Hart and Strathmann, 1994; McAlister and Miner, 2017; Soars et al., 2009). In juveniles and adults, there are only a few studies that have assessed plasticity of sea urchin tube feet (Cohen-Rengifo et al., 2017; Santos et al., 2005).

Sea urchin tube feet are terminal extensions of the water vascular system and are fundamental for survival. They are used for locomotion, sensing, feeding, respiration, and adhesion to the substrate (Lawrence, 1987; Lesser et al., 2011). Each tube foot is connected to the water vascular system with an internal ampulla (Smith, 1978) which functions as a muscular bladder and connects to an external retractable stalk (stem) that terminates in an adhesive disc (see Fig. 1 in Santos et al., 2013). During extension, fluid is forced into the tube foot stem and it elongates; during contraction, water moves out of the stem back into the ampulla. During this process, the flattened adhesive disc contacts and can adhere to the substratum. Adhesion is generated by a duo-gland adhesive system present in the epidermis of the disc that releases adhesive (glue) and de-adhesive secretions, allowing for temporary adhesion to the substrate as a sea urchin clings to or ambulates across (Flammang, 1996).

Attachment strength of tube feet depends, among other factors, on: number of tube feet used to adhere, adhesive secretion, tensile strength (i.e., force per unit area) of the disc, and breaking force of the stem (Cohen-Rengifo et al., 2017; Santos and Flammang, 2007, Santos and Flammang, 2008; Sharp and Gray, 1962; Smith, 1978). The degree of specialization, shape, and mechanical properties of tube feet differs inter- and intra-specifically (Fenner, 1973; Leddy and Johnson, 2000; Santos and Flammang, 2008; Santos and Flammang, 2007; Santos and Flammang, 2006; Smith, 1978). For example, in some species the total number of tube feet is higher in larger urchins, potentially improving attachment capacity (Connolly et al., 2017; Strathmann and von Dassow, 2001). In other species, tube feet morphology differ as a function of body location, where oral tube feet (in direct contact with substrate) have thicker stem walls and larger disc area for better attachment strength, while aboral tube feet (extended into the water column) have thinner stem walls and reduced disc area to enhance respiration (Fenner, 1973; Leddy and Johnson, 2000). In Holopneustes purpurascens, tube feet attachment capacity and morphology are similar in all body locations (Connolly et al., 2017). Thus, tube foot adhesive properties and morphology differ significantly among and within species (Santos et al., 2005; Santos and Flammang, 2006, Santos and Flammang, 2007, Santos and Flammang, 2008). However, the plasticity of tube feet adhesion and morphology in response to environmental factors is less understood.

Secure attachment is critical for sea urchins living in hydrodynamically intense open coast intertidal and shallow reefs. During high tide, wave-induced water motion exerts large hydrodynamic forces (Denny, 1988). Unlike mussels and barnacles that attach permanently, and limpets that maintain continuous attachment (i.e., transitory attachment), sea urchins attach temporarily, adhering and releasing tube feet while they feed and locomote in this dynamic environment (reviewed in Dodou et al., 2011). However, tube feet do not always release. When subjected to extreme tensional stress, e.g., from strong wave forces, the stem can catastrophically fail and leave the disc and a portion of the stem attached to the substrate (Santos and Flammang, 2005; Smith, 1978). Surprisingly, there is little research on several key behavioral aspects of tube feet attachment (e.g., the dynamics of intra- and inter-specific variation of glue utilization, and incidence of tube feet breakage in the wild).

The frequency of tube feet amputation in wild populations is difficult to determine, as regeneration does not leave scars in the tissue, and visual examination of tube feet regeneration can be challenging (Lindsay, 2010). However, observations of amputated tube feet from live sea urchins torn from the substrate have been reported (Santos and Flammang, 2005; Smith, 1978) and high seawater velocity during a storm event can dislodge urchins from the substrate (Siddon and Witman, 2003), probably amputating tube feet. We have also observed the amputation of tube feet when collecting urchins from different rock substrates at many field sites (pers. obs.). Compromised integrity of tube feet, in terms of the total number available for attachment and functionality (i.e., ability to attach), will negatively impact sea urchin feeding, locomotion, and sensory perception. Consequently, fast recovery of amputated tube feet is critical for survival. The few studies that have focused on sea urchin tube feet regeneration have investigated genetic and mechanistic attributes (Bodnar and Coffman, 2016; Brown and Caldwell, 2017; Loram and Bodnar, 2012; Reinardy et al., 2015), but studies on the functional and ecological aspects of tube foot regeneration are lacking. For example, it is unknown if there is a size-related regeneration rate, the regeneration time, the size of the amputated adhesive disc, and when the tube foot regains its pre-amputation functionality.

Post-metamorphic echinoids show a high degree of phenotypic plasticity in variable environments. When food increases, urchins can increment gonad production (Russell, 1998) and increase the size of feeding apparatus (Black et al. 1982; Walker 1981; but see DeVries and Taylor, 2019 for an alternative explanation in Strongylocentrotus purpuratus). In the presence of predators, some urchin species increase the thickness of their test (Selden et al., 2009), while others reduce their foraging behavior (Freeman, 2006; Kintzing and Butler, 2014; Matassa, 2010). The purple sea urchin, Strongylocentrotus purpuratus, increases gonad size when food becomes available (Russell, 1998) and alter its test profile (Height to Diameter ratio) depending on the size of the pits they burrow and inhabit (Hernández and Russell, 2010; Russell et al., 2018). These test shape differences are driven by exposure and the ability to bore protective pits in intertidal rocks (Hernández and Russell, 2010; Russell et al., 2018). Urchins boring pits on hard, smooth, metamorphic granite, exhibit lower profiles than those on smooth, soft mudstone and rough, soft sandstone. Substrate complexity and rugosity also impacts urchin ability to attach (Santos et al., 2005) and recruit to the substrate (Clemente et al., 2013). Given the variation in natural rock substrates that S. purpuratus inhabits and the plasticity associated with it, it is likely that substrate lithology will affect the morphology of tube feet, particularly its disc area.

In this study, we assessed the influence of two substrates with contrasting rugosity – smooth mudstone, and medium-grain sandstone – on tube foot disc surface area by evaluating two urchin populations found on sites with different substrates (in-situ). We also evaluated the ecological consequence of regeneration and the role of plasticity during this process by assessing the timeline of tube foot regeneration functionality and performance. In the laboratory (ex-situ), we measured length, disc appearance, adhesive force, and disc area of tube feet during the regeneration process. Our results provide a new perspective into phenotypic plasticity and the basic functional morphology of sea urchin tube foot regeneration.

Section snippets

Disc surface area in situ

To examine how disc surface area (mm2) relates to the native substrate, sea urchin size (i.e. diameter), and body location (oral/aboral), we collected Strongylocentrotus purpuratus on February 26, 2018, from two different types of intertidal rocks. The sandstone at Bean Hollow (37° 13′ 36.08″ N 122° 24′ 41.70″ W) is approximately 50% quartz, 35% feldspar and 15% lithic fragments. The grain shapes are sub-angular to sub-rounded and weakly to moderately cemented by amorphous silica (Russell et

Disc area in the field

Mean disc surface area differed among collection sites, sea urchin body location, and sea urchin size. There was no significant interaction among any of the factors (Table 1). Sea urchins from Palomarin (native to mudstone) had larger disc surface area (Fig. 2), across all sizes and body locations than urchins collected in Bean Hollow (native to sandstone). The mean surface area of oral discs was larger than aboral discs for both sites and all urchin sizes. Finally, the mean disc surface area

Discussion

Our study shows that tube feet are plastic in nature. In-situ (field), we found population-level differences in disc surface area and, in ex-situ conditions, urchins did not recover their pre-amputation functional morphology. Moreover, tube feet of ambulacral columns that were not amputated showed phenotypic plasticity by reducing their disc surface area, but not length, over time. Tube feet amputation had long-lasting consequences in Strongylocentrotus purpuratus. Urchins regained a minimum

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed.

Declaration of Competing Interest

Author declares that they have no conflict of interest.

Acknowledgments

We thank Villanova University students Lukas Troha, Marielle Dineen-Carey, Prisca To, Ben Ellison, and Daniel Scutella for laboratory assistance. Leonardo Miranda for helping with the experimental setup. Three anonymous reviewers provided careful and critical commentary that significantly improved the manuscript. Biology department of Villanova University for their resources and funding. National Science Fundation (NSF OCE-0623934)

References (61)

  • J.D. Urriago et al.

    Responses of the black sea urchin Tetrapygus niger to its sea-star predators Heliaster helianthus and Meyenaster gelatinosus under field conditions

    J. Exp. Mar. Bio. Ecol.

    (2011)
  • M.D. Abramoff et al.

    Image processing with ImageJ

    Biophoton. Int.

    (2004)
  • D.K. Adams et al.

    Rapid adaptation to food availability by a dopamine-mediated morphogenetic response

    Nat. Commun.

    (2011)
  • R. Black et al.

    Relative size of Aristotle's lantern in Echinometra mathaei ocurring at different densities

    Mar. Biol.

    (1982)
  • C.A. Blanchette et al.

    Biogeographical patterns of rocky intertidal communities along the Pacific Coast of North America

    J. Biogeogr.

    (2008)
  • A.G. Bodnar et al.

    Maintenance of somatic tissue regeneration with age in short- and long-lived species of sea urchins

    Aging Cell

    (2016)
  • L.R. Brown et al.

    Tissue and spine regeneration in the temperate sea urchin Psammechinus miliaris

    Invertebr. Reprod. Dev.

    (2017)
  • S. Clemente et al.

    Predators of juvenile sea urchins and the effect of habitat refuges

    Mar. Biol.

    (2013)
  • M. Cohen-Rengifo et al.

    Attachment capacity of the sea urchin Paracentrotus lividus in a range of seawater velocities in relation to test morphology and tube foot mechanical properties

    Mar. Biol.

    (2017)
  • M. Cohen-Rengifo et al.

    Ocean warming and acidification alter the behavioral response to flow of the sea urchin Paracentrotus lividus

    Ecol. Evol.

    (2019)
  • D.M. Connolly et al.

    Influence of body size on tube feet morphology and attachment capacity in the sea urchin Holopneustes purpurascens (Temnopleuridae)

    Mar. Biol.

    (2017)
  • R. Core Team

    R: A Language and Environment for Statistical Computing

    (2019)
  • K. Crook et al.

    Influence of spawning capelin Mallotus villosus on the distribution of green sea urchins Strongylocentrotus droebachiensis on the Northeast Newfoundland coast

    Mar. Ecol. Prog. Ser.

    (2016)
  • M.W. Denny

    Biology and the Mechanics of the Wave-Swept Environment

    (1988)
  • M.S. deVries et al.

    Re-examination of the effects of food abundance on jaw plasticity in purple sea urchins

    Mar. Biol.

    (2019)
  • T.J. DeWitt et al.

    Phenotypic variation from single genotypes

  • D. Dodou et al.

    Mechanisms of temporary adhesion in benthic animals

    Biol. Rev.

    (2011)
  • T.A. Ebert

    Adaptive aspects of phenotypic plasticity in echinoderms

    Oceanol. Acta

    (1996)
  • C.E. Emerson et al.

    Ocean acidification impacts spine integrity but not regenerative capacity of spines and tube feet in adult sea urchins

    R. Soc. Open Sci.

    (2017)
  • D.H. Fenner

    The respiratory adaptations of the podia and ampullae of echinoids (Echinodermata)

    Biol. Bull.

    (1973)
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