Barrens of gold: gonad conditioning of an overabundant sea urchin

Overgrazing by the overabundant native purple urchin Heliocidaris erythrogramma has caused kelp-dominated reefs to shift to urchin barrens throughout southeastern Australia. These areas are characterised by low kelp abundance, low biodiversity and high urchin densities. As purple urchin gonads are a delicacy in many countries, commercial harvest from barrens could aid kelp recovery. However, the lack of macroalgae in these habitats, driven by high urchin densities, results in urchins with small, poor-quality roe that is commercially undesirable. To overcome this, we assessed whether urchin gonad quantity and quality could be improved with access to high-quality feed and optimal environmental conditions, a process known as &lsquo;gonad conditioning&rsquo;. Specifically, we (1) surveyed the quality of urchins from barrens and kelp sites in Port Phillip Bay, Australia, over 18 mo and (2) tested if gonad conditioning was effective on urchins from barrens during and after the harvest season. Field surveys revealed considerable variation in gonad size across sites, habitats and collection periods (mean gonad index range: 3 to 12%). Gonad conditioning with the best diet increased urchin gonad size by up to 2.8 times during the harvest season. Moreover, gonads of conditioned urchins from one barren were 3 times brighter in colour and contained lower concentrations of arsenic than wild urchins. In contrast, gonad conditioning at 22&deg;C after the harvest season was ineffective. Our results show that targeted in-season harvest from barrens and subsequent gonad conditioning produces roe of commercial quality, promoting the use of urchin fisheries as a tool for managing urchin barrens.<br /

Beeinflusst Umweltstress die Verteidigungsfähigkeit von marinen Makroalgen gegen Fraß und Aufwuchs?

Makroalgen sind wichtige Primärproduzenten in den euphotischen Zonen derKüstenbereiche. Durch anthropogene Einflüsse werden diese Ökosysteme starkbedroht, so kommt es vielerorts zu einer zeitweiligen oder permanenten Wassertrübung durch z. B. erhöhte Sedimentation oder Eutrophierung. Beides führtdazu, dass die Eindringtiefe des Sonnenlichts verringert wird und somit die Algen weniger Licht zur Verfügung haben. Durch diesen Lichtmangel können Algen gestresst werden und sind somit anfälliger gegenüber Fraßfeinden oder Epibionten aller Art. Meine Diplomarbeit beschäftigt sich damit, inwiefern sich die Verteidigung von Makroalgen mit zunehmendem Lichtmangelstress verändert. Der Hintergrund war die Annahme, dass die Bildung besonders von chemischen Fraßschutzmitteln energieaufwendig für Pflanzen ist. Die Folge daraus ist, dass der Alge mit zunehmendem Stress weniger Energie für ihre Verteidigung zur Verfügung steht, da sie die ihr verbleibende Energie in den Erhalt ihrer Biomasse investieren muss. Um dies zu überprüfen, wurden Algen durch Lichtmangel gestresst und anschließend auf ihre Attraktivität auf Konsumenten bzw. auf eine chemische Aktivität gegenüber Makro- und Mikroepibionten untersucht. Einzelne Algenindividuen wurden unter verschiedenen Lichtintensitäten gehältert um anschließend zu testen, ob die Stärke der Verteidigung eine Funktion des Lichtmangels ist. Untersucht wurden 2 Braunalgen: Zonaria turneriana (Dictyotales) und Carpoglossum confluens (Fucales). Mit Algenmaterial beider Arten wurden nach der Stressinduktion folgende Versuche durchgeführt: Fraßversuche mit Paridotea ungulata (Isopoda), Antifoulingtests mit Mytilus edulis (Bivalvia) und bakterielle Inhibitionsversuche. Bei keiner der beiden Arten konnte jedoch ein signifikanter Zusammenhang zwischen den verwendeten Lichtintensitäten und der Verteidigung gegen Konsumenten oder Epibionten festgestellt werden. Auch der Vergleich der Mittelwerte der verschiedenen Antwortvariablen zeigte keine signifikanten Unterschiede zwischen den Lichtintensitäten auf. Bei Z. turneriana wurde das Vorhandensein einer Verteidigung gegen alle drei Organismengruppen festgestellt, jedoch war diese nicht abhängig von den Lichtbedingungen, unter denen die Algen gehältert wurden. Die Versuche mit C. confluens zeigten hingegen keinen Hinweis auf eine chemische Verteidigung und es wurden keine Unterschiede bezüglich der Verteidigungsfähigkeit zwischen den Algen aus den unterschiedlichen Lichtintensitäten gefunden. Die Ergebnisse meiner Arbeit unterstützen nicht die Theorie, dass die Bildung von chemischer Verteidigung energieaufwendig ist

Percentage cover of turf-forming algae <i>versus</i> cover of canopy-formers.

<p>Open circles display reefs with ambient nutrient conditions and filled circles are reefs with enhanced nutrient levels across all experimental patch reefs at the conclusion of the 13 months experiment (the treatment of ‘reef state’ is not indicated). Fitted line represents treatments pooled across ambient and enhanced nutrient reefs (<i>R</i>² = 0.75, y = -0.056x + 4.16, values derived from linear regression with transformation ln(Y)) because a 1-way ANCOVA showed no significant difference in relationships between reefs with enhanced nutrients and those with ambient nutrient levels (homogeneity of slopes: <i>F</i>_1,24 = 0.85, <i>P</i> = 0.36; test between treatments after factoring for the covariate, <i>F</i>_1,25 = 1.00, <i>P</i> = 0.33).</p

Phase-Shift Dynamics of Sea Urchin Overgrazing on Nutrified Reefs

<div><p>Shifts from productive kelp beds to impoverished sea urchin barrens occur globally and represent a wholesale change to the ecology of sub-tidal temperate reefs. Although the theory of shifts between alternative stable states is well advanced, there are few field studies detailing the dynamics of these kinds of transitions. In this study, sea urchin herbivory (a ‘top-down’ driver of ecosystems) was manipulated over 12 months to estimate (1) the sea urchin density at which kelp beds collapse to sea urchin barrens, and (2) the minimum sea urchin density required to maintain urchin barrens on experimental reefs in the urbanised Port Phillip Bay, Australia. In parallel, the role of one of the ‘bottom-up’ drivers of ecosystem structure was examined by (3) manipulating local nutrient levels and thus attempting to alter primary production on the experimental reefs. It was found that densities of 8 or more urchins m^-2 (≥ 427 g m^-2 biomass) lead to complete overgrazing of kelp beds while kelp bed recovery occurred when densities were reduced to ≤ 4 urchins m^-2 (≤ 213 g m^-2 biomass). This experiment provided further insight into the dynamics of transition between urchin barrens and kelp beds by exploring possible tipping-points which in this system can be found between 4 and 8 urchins m^-2 (213 and 427 g m^-2 respectively). Local enhancement of nutrient loading did not change the urchin density required for overgrazing or kelp bed recovery, as algal growth was not affected by nutrient enhancement.</p></div

<i>E</i>. <i>radiata</i> recruitment.

<p>Abundance (mean ± SE) of <i>E</i>. <i>radiata</i> recruits on reefs above and below the critical urchin density (4 urchins m^-2) for kelp recovery after 13 months (‘Kelp’ and ‘Barrens’ refers to the initial states of reefs). Nutrient enhancement did not influence recruitment and therefore data for ‘nutrient enhanced’ and ‘ambient nutrient’ reefs were pooled for display.</p

Dependence of algal species richness and diversity on canopy cover.

<p>Panel a) details cover of canopy-forming algae, b) shows macroalgal species richness, and c) macroalgal species diversity, against sea urchin densities at the end of the 13 month experimental period. Reefs with initial states of ‘kelp bed’ and ‘urchin’ barrens’ are indicated by a grey circle and a white triangle respectively; data are means ± SE. Reefs with enhanced nutrients have been pooled with reefs with ambient nutrient conditions since the addition of fertiliser did not influence response variables (see Tables <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0168333#pone.0168333.t002" target="_blank">2</a> and <a href="http://www.plosone.org/article/info:doi/10.1371/journal.pone.0168333#pone.0168333.t003" target="_blank">3</a>). Note that species present at the start of the experiment (<i>E</i>. <i>radiata</i> for kelp bed reefs and encrusting red algae for all reefs) were excluded from the analysis. Arrows in (a) show responses to experimental manipulation of sea urchin biomass in kelp beds (thick grey arrows = forward-shift ‘collapse’ from kelp to urchin barrens) and on sea urchin barrens (thin black arrows = reverse-shift ‘recovery’ from urchin barrens back to kelp beds).</p

Results of 2-way fixed effects model I Analysis of Covariance testing the significance of differences in responses of species richness (a) and Shannon diversity (b) across different urchin densities (covariate), dependent on initial ‘reef state’ (kelp <i>vs</i>. barrens) and nutrient conditions (ambient <i>vs</i>. enhanced) after 13 months of treatment.

<p>Results of 2-way fixed effects model I Analysis of Covariance testing the significance of differences in responses of species richness (a) and Shannon diversity (b) across different urchin densities (covariate), dependent on initial ‘reef state’ (kelp <i>vs</i>. barrens) and nutrient conditions (ambient <i>vs</i>. enhanced) after 13 months of treatment.</p

Results of 1-way fixed effects model I Analysis of Covariance testing the differences in cover of canopy-forming macroalgae at different urchin densities (covariate) and nutrient conditions (ambient <i>vs</i>. enhanced) for the 4 periods of <i>a priori</i> interest across a quarter (3 months), half (6 months), three quarters (9 months) and a full year (13 months).

<p>Results of 1-way fixed effects model I Analysis of Covariance testing the differences in cover of canopy-forming macroalgae at different urchin densities (covariate) and nutrient conditions (ambient <i>vs</i>. enhanced) for the 4 periods of <i>a priori</i> interest across a quarter (3 months), half (6 months), three quarters (9 months) and a full year (13 months).</p

Kelp collapse and recovery at different urchin densities over time.

<p>Percentage cover of canopy-forming algae at a range of sea urchin densities (individuals m^-²) on patch reefs initiated as the ‘kelp bed’ (a) and (b), and ‘barrens’ state (c) and (d) in northern Port Phillip Bay, Nov. 2012 to Dec. 2013. Plots (a) and (c) represent reefs with ambient nutrient levels, and (b) and (d) show results for reefs with enhanced nutrient levels.</p