Investigating diets of Centrostephanus rodgersii and their suspected key predators on temperate subtidal reefs; Who seems to be in control?

Sea urchins play a significant role in structuring marine food-webs as herbivores and prey. When occurring in large numbers they can create "barrens", areas devoid of macroalgae and considered to be low-productivity environments. Generally, urchins are thought to show reduced body condition in barrens due to the lack of macroalgal food leading to poor gonad (or 'roe') quality, prohibiting their reproduction. However, many urchins are omnivores rather than obligate macroalgal specialists, so they may avail themselves of more diverse resources. Abundant predators like lobsters and fishes may control urchin populations thereby reducing barrens, although this is only thought to occur with the presence of large-bodied predators. Trophic information on Centrostephanus rodgersii (long-spined urchin) and the species suggested to be its "key" predators, Sagmariasus verreauxi (eastern rock lobster), Achoerodus viridis (eastern blue groper) and Chrysophyrus auratus (pink snapper) in southeastern Australia is scant. The focus of this PhD was to investigate C. rodgersii food-webs via gut contents (Chapters 2 and 6), stable isotope analysis (Chapter 3) and feeding trials (Chapters 4 and 5) to provide insight into the role of C. rodgersii in temperate rocky reef systems and the potential for predators to regulate urchin populations. In Chapter 1, I provide a general introduction to the topic of urchin grazing and the expansion of C. rodgersii in southeastern Australia, covering general concepts regarding urchin diets worldwide and potential for C. rodgersii diets to not be restricted to macroalgae alone. I also describe the generally accepted conceptual models regarding predator control of C. rodgersii by lobsters and large fishes and contrast with international comparisons.

In Chapter 2, gut contents and gonad analysis of 150 C. rodgersii collected over > 470 km of the NSW coastline, in barrens and macroalgal forests, showed that urchins are omnivores whose diets feature various macroalgae (85–100 %) and invertebrates (63–77 %) irrespective of habitat. In most comparisons (80 %), urchins in nearshore barrens were equally healthy based on gonad weight as those in macroalgal forests. These results do not align with interpretations of C. rodgersii as obligate macroalgal specialists as reported previously and show that urchins energetic requirements can be met in barrens.

Stable isotope analysis, and the associated metrics, have been routinely used to investigate food web characteristics of many marine species. Isotopic niche analysis (Chapter 3) showed substantial overlap (81– 97%) in C. rodgersii resource use between barrens and macroalgal habitats, challenging the notion of nutritional deficiency in barrens. However, isotopic niche size was reduced on average in barrens by approximately half suggesting that resources can indeed be limited, though due to dietary breadth this is not always the case. The isotopic niche analysis and gut contents data align, indicating that C. rodgersii is a generalist omnivore in multiple habitats.

In Chapter 4, mesocosm trials of up to 76 days with 120 urchins showed unexpectedly low rates of S. verreauxi predation (32.5 %). Lobsters were seen to be capable but hesitant urchin predators and primarily ate small urchins < 70 mm Test Diameter (TD). Surprisingly, small lobsters ate significantly more urchins than large lobsters > 120 mm Carapace Length (CL). I found no physical limitation for small lobsters (104 mm CL) eating large urchins (90 mm TD) in the successive trials, challenging the notion that only large lobsters are effective predators of urchins.

Tethering studies with 100 urchins over 25 nights (Chapter 5) confirmed S. verreauxi exhibited low predation rates (4 %) while Heterodontus spp. sharks ate more urchins (45 %). Notably, lobsters were often filmed walking past tethered urchins in search of other food, and this occurred despite undertaking the experiment at an inhabited lobster den where lobsters are plentiful, and predators congregate. Comparatively, sharks readily consumed urchins eating many large C. rodgersii > 120 mm TD. These results align with Chapter 4 (mesocosm trials) as the data from both of these chapters challenges the notion of depauperate C. rodgersii predators in NSW. Finally, the gut contents of two (2) key temperate rocky reef predators were investigated (Chapter 6). The gut contents of 39 A. viridis (blue groper) and 111 C. auratus (snapper) collected > 1250 km of NSW coastline showed few occurrences of C. rodgersii for either A. viridis or C. auratus (~ 5 % and 3 %, respectively). Snails (~ 87 and 47 %), macroalgae (~ 66, 69 %), crabs (~ 59, 46 %) and other urchins (~ 31, 13 %) occurred more frequently than C. rodgersii for A. viridis and C. auratus, respectively. Interestingly, predator size effects were absent or inconsistent between latitudes. These results do not align with previous interpretations of large fishes as key predators that control C. rodgersii populations.

Overall, my findings indicate that food-web dynamics of C. rodgersii are more nuanced than previously considered. I found urchins to be generalist omnivores with high isotopic niche overlap in both habitats, rejecting the assertion that C. rodgersii are obligate macroalgal specialists. This suggests the overall impact of urchins on macroalgal forests in NSW may be overstated. I also found no clear agent of urchin predatory "control" by large lobsters or fishes, or a single key species that is likely to regulate C. rodgersii. Surprisingly, small lobsters and Heterodontus spp. sharks ate most of the urchins in feeding trials, indicating that C. rodgersii predators are more varied than previously reported. This work describes a higher level of food web complexity for C. rodgersii and its predators than has been presented so far. As such, the causative links between predator and urchin populations in southeastern Australia are brought into question, highlighting the need for further investigation into their respective roles in temperate marine ecosystems.