Dataset

Drift-kelp suppresses foraging movement of overgrazing sea urchins

University of Tasmania, Australia
Kriegisch, Nina ; Ling, Scott, Dr ; Reeves, Simon
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ctx_ver=Z39.88-2004&rft_val_fmt=info%3Aofi%2Ffmt%3Akev%3Amtx%3Adc&rfr_id=info%3Asid%2FANDS&rft_id=https://metadata.imas.utas.edu.au:443/geonetwork/srv/en/metadata.show?uuid=fa687839-5e4b-4d34-a8f2-6ad37cfb4e30&rft.title=Drift-kelp suppresses foraging movement of overgrazing sea urchins&rft.identifier=https://metadata.imas.utas.edu.au:443/geonetwork/srv/en/metadata.show?uuid=fa687839-5e4b-4d34-a8f2-6ad37cfb4e30&rft.publisher=Institute for Marine and Antarctic Studies, University of Tasmania&rft.description=Sea urchins have the capacity to destructively overgraze kelp beds and cause a wholesale shift to an alternative and stable ‘urchin barren’ state. However, their destructive grazing behaviour can be highly labile and contingent on behavioural shifts at the individual and local population level. Changes in supply of allochthonous food sources, i.e. availability of drift-kelp, is often suggested as a proximate trigger of change in sea urchin grazing behaviour, yet field tests of this hypothesis are rare. Here we conduct a suite of in situ behavioural surveys and manipulative experiments within kelp beds and on urchin barrens to examine foraging movements and evidence for a behavioural switch to an overgrazing mode by the Australian sea urchin Heliocidaris erythrogramma (Echinometridae). Tracking of urchins using time-lapse photography revealed urchin foraging to broadly conform to a random-walk-model within both kelp beds and on barren grounds, while at the individual level there was a tendency towards local ‘homing’ to proximate crevices. However, consistent with locally observed ‘mobile feeding fronts’ that can develop at the barrens-kelp interface, urchins were experimentally inducible to show directional movement toward newly available kelp. Furthermore, field assays revealed urchin grazing rates to be high on both simulated drift-kelp and attached kelp thalli on barren grounds, however drift-kelp but not attached kelp was consumed at high rates within kelp beds. Time-lapse tracking of urchin foraging before/ after the controlled addition of drift-kelp on barrens revealed a reduction in foraging movement across the reef surface when drift-kelp was captured. Collectively results indicate that the availability of drift-kelp is a pivotal trigger in determining urchin feeding modes, which is demonstrably passive and cryptic in the presence of a ready supply of drift-kelp. Recovery of kelp beds therefore appears possible if a sustained influx of drift-kelp was to inundate urchin barrens, particularly on reefs where local urchin densities and where grazing pressure is close to the threshold enabling kelp bed recovery.The study was carried out in the semi-enclosed coastal environment of Port Phillip Bay (PPB) in SE Australia, where H. erythrogramma is the most influential herbivore on shallow rocky reefs and demonstrates both ‘passive’ (feeding on drift-kelp) and active (feeding on attached seaweeds) forms of foraging. To assess urchin foraging dynamics, 4 different experiments were conducted across 4 regions of PPB. The regions represented a gradient in urchin overgrazing impacts from relatively small barrens patches of 10-100s m2 within kelp beds typical of southern regions, to extensive ‘continuous’ barrens stretching over 100,000s m2 of sub-tidal reef in northern and western regions. In the north, kelp beds predominantly feature Ecklonia radiata, with only sparse growth of fucoid species (Sargassum spp. and Cystophora spp.) whereas in the southern regions kelp beds show more fucoid algae and a more developed understory. The underlying reef substratum was consistent across all regions, occurring as mixed boulder / flat rock reef interspersed by sand patches to a depth of 5.5 m. Directional movement of urchins towards attached kelp Experimental design: This ‘choice’ experiment was conducted in April 2014 in the north of PPB on barrens habitat (depth range 3 – 4 m). Single urchins, situated on the top of large flat boulders, were randomly chosen for use in the trials. Six dive weights were placed equidistantly at a radius of 200 mm around each selected urchin taking care not to disturb the urchins. The dive weights alternatingly held down pieces of kelp (E. radiata) and surrogate kelp (brown cloth) folded in half in such a way that the two free ends faced the urchin. The cloth surrogate was similar in structure, colour and size to the E. radiata pieces. The dive weights were coated in epoxy and both the weights and surrogate cloth were preconditioned on the sea floor for 2 months prior to start of the experiment to mitigate potentially negative effects of any unknown leachates. Hydrodynamic conditions were monitored with an additional dive weight holding a light piece of plastic tape 10cm in length which was position just within the field of view of the camera. During all trials water movement was slightly tidal, this means that there was low movement towards the shore and from shore. To differentiate urchin choice between natural vs surrogate kelp, the trials were monitored with time-lapse photography. A camera (Panasonic Lumix DCM TS4 in underwater housing) was placed on a 1 to 1.5 m tall tripod fixed to the benthos with tie-downs, and set to take still shots of the trial every 15 mins over a 15 hour period (pilot trials indicated that a time-lapse frequency of 15 mins sufficiently captured the slow urchin movement dynamics). The period of 15 hours was chosen to ensure that the choice the urchin made was captured with the camera During trial set-up, individual urchins were neither touched nor moved. A total of 11 replicate trials on different urchin individuals were conducted, all of which were started at midday. A ‘choice’ was recorded when the urchin moved to the kelp or to the surrogate and stayed at that position for more than 30 min (2 consecutive time-lapse images) or alternatively moved entirely out of the field of view, at which point the trial was deemed to have resulted in ‘nil choice’. Movement rates of urchins in different regions and habitats Experimental design: Movement of H. erythrogramma was assessed periodically using time-lapse photography from summer 2012 to summer 2014 in the western, northern and southeastern regions of PPB. To monitor movement of urchins, 4 time-lapse cameras were used as described above. In this experiment, the frequency of photographs was every 5 minutes and each sequence was 5 hours in duration (i.e. 60 images in total). This was done to adequately capture changes in direction and speed of individual urchins. These sequences were taken in each region, in kelp and barrens habitat if both habitats were present. Six replicate time-lapse sequences were taken in each habitat and in each region during the 2 years (2012 – 2014, n = 30 sequences). Each sequence was photographed on a unique patch of reef containing unique urchin individuals to maintain independence of replicate sequences. Criteria for identifying suitable locations in barrens and kelp habitat were that the reef had low topographic relief with high densities of urchins able to be squarely framed within the camera’s field of view. For each image sequence, an object of known dimensions was photographed to enable calibrating the dimensions of the field of view. Preliminary trials were run at night in the north and southeast in barrens habitat to assess movement across the entire diel cycle. Trials conducted during the day and night (4 replicates for the night and 5 for the day period; n = 9) revealed no significant difference of movement between day and night for the different regions. For photographing at night the flash of the cameral was used, this was considered to have little effect on the urchins. All subsequent monitoring of urchins was therefore performed during daylight hours, which increased ease of camera deployments and retrievals. Kelp consumption rates in different habitats Experimental design: A standardised assay of sea urchin herbivory was used to compare rates and types of feeding behaviour of urchins on different types of kelp food sources on barrens and in kelp beds, across the 4 different regions of PPB during March 2014. Following the protocol of Vanderklift and Wernberg (2008), assays in kelp and barrens habitats in the same region occurred at a minimum separation distance of 50 m, to ensure the urchin populations were independent based on maximum urchin movement rates over the duration of the assay. Prior to the start of the assays, urchin densities/m2 and biomass/m2 were defined for each habitat (Table 2) from a sample of 8 randomly chosen replicate quadrats (1 m2). Densities were converted to biomass by estimating the mean test diameter from n = 10 urchins in each region and habitat, and converting this to biomass based on the relationship between test diameter and weight calculated for each region / habitat (this relationship was determined from 48 – 90 urchins sampled randomly throughout the entire bay). To simulate the different types of kelp food sources (attached kelp on the benthos, drift kelp on the benthos, the canopy of attached kelp elevated away from the substratum, and caged kelp as a control) pieces of kelp were tethered to metal chain in different ways. To mimic attached kelp on the benthos accessible to sea urchins (and any other benthic herbivores), kelp pieces were fastened directly to the chain with clothes pegs. For simulation of drift-kelp, light nylon monofilament fishing line was attached to pieces of chain and a piece of kelp was held in place by a clothes peg at the other end of the fishing line. To examine the amount of fish grazing on kelp, pieces of kelp were fastened as per mimicking drift-kelp, but additionally with a float so that the kelp lamina floated at canopy height and was not accessible to urchins. To account for loss of algae due to tissue degradation and erosion (i.e. the ‘control’ treatment), another set of kelp pieces were fastened directly to the chain and protected with small plastic cages of mesh size 5 mm. Given the short duration of the experiment it was assumed that the lightweight cages did not affect the area of the kelp pieces within them. Each treatment had 12 replicates (48 pieces of algae in total) and the experiment was run for 3 days. The standardised kelp pieces used in the assays, i.e. 50 mm lengths of clean healthy lateral frond tissue of E. radiata with no visible epiphytes, were freshly harvested on the day of the experiment. To determine kelp loss over the duration of the experiment, the kelp pieces were photographed both prior to and at the conclusion of the assay. Kelp pieces were held flat by pressing the sample between a clear Perspex sheet and an opaque sheet and photographed. The change in kelp area was calculated using the freeware ImageJ as a proxy to estimate rates of consumption (the area of the ‘control’ pieces did not change over the course of the experiment). To convert consumption rates as planar area to biomass, 10 kelp sections ranging in size were taken to the laboratory, photographed and wet weights taken in order to calculate biomass per unit area. Behavioural response of sea urchins to drift-kelp availability Experimental design: The change in activity of H. erythrogramma associated with the presence / absence of drift-kelp was monitored using time-lapse photography. The experiment was implemented as a before-after control-impact (BACI) design, whereby urchin movement within a total of eight plots of ~ 0.6 m2 on barrens habitat was monitored before and after the addition of drift-kelp to treatment plots (n = 4) alongside control plots (n = 4) to which no drift-kelp was added. The experiment was conducted during October 2014, with the BACI design involving an initial 4 hours of tracking before the drift-kelp treatment was added and then a subsequent 4 hours of tracking following the application of kelp. The treatment involved gently placing drift-kelp against all sea urchins within the field of view of the camera and within a 0.5 m buffer zone surrounding the camera field of view. Upon detection of the drift-kelp (a fresh cut lateral of E. radiata) urchins invariably extended their tube feet and seized the piece, which typically took on the order of 10 seconds.&rft.creator=Kriegisch, Nina &rft.creator=Ling, Scott, Dr &rft.creator=Reeves, Simon &rft.date=2019&rft.coverage=northlimit=-38.2143715314; southlimit=-38.2234075714; westlimit=145.027009964; eastLimit=145.031988144&rft.coverage=northlimit=-37.8694937453; southlimit=-37.8707810922; westlimit=144.889723778; eastLimit=144.896332741&rft.coverage=northlimit=-38.0271103801; southlimit=-38.0333302808; westlimit=144.570177875; eastLimit=144.58322414&rft.coverage=northlimit=-38.1472868037; southlimit=-38.1591657375; westlimit=144.730998787; eastLimit=144.746448311&rft_rights=Attribution 4.0 International http://creativecommons.org/licenses/by/4.0/&rft_rights=The data described in this record are the intellectual property of the University of Tasmania through the Institute for Marine and Antarctic Studies.&rft_subject=biota&rft_subject=sea urchin barrens&rft_subject=time-lapse&rft_subject=regime shift&rft_subject=foraging behaviour&rft_subject=Heliocidaris erythrogramma&rft_subject=Ecklonia radiata&rft_subject=Temperate Reef&rft_subject=EARTH SCIENCE | BIOSPHERE | ECOSYSTEMS | MARINE ECOSYSTEMS&rft_subject=EARTH SCIENCE | BIOSPHERE | ECOSYSTEMS | MARINE ECOSYSTEMS | BENTHIC&rft_subject=EARTH SCIENCE | BIOSPHERE | ECOSYSTEMS | MARINE ECOSYSTEMS | REEF&rft_subject=EARTH SCIENCE | BIOSPHERE | ECOSYSTEMS | MARINE ECOSYSTEMS | COASTAL | KELP FOREST&rft_subject=Marine and Estuarine Ecology (incl. Marine Ichthyology)&rft_subject=BIOLOGICAL SCIENCES&rft_subject=ECOLOGY&rft_subject=Ecosystem Function&rft_subject=ENVIRONMENTAL SCIENCES&rft_subject=ECOLOGICAL APPLICATIONS&rft_subject=Fisheries Management&rft_subject=AGRICULTURAL AND VETERINARY SCIENCES&rft_subject=FISHERIES SCIENCES&rft.type=dataset&rft.language=English Access the data

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The data described in this record are the intellectual property of the University of Tasmania through the Institute for Marine and Antarctic Studies.

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Sea urchins have the capacity to destructively overgraze kelp beds and cause a wholesale shift to an alternative and stable ‘urchin barren’ state. However, their destructive grazing behaviour can be highly labile and contingent on behavioural shifts at the individual and local population level. Changes in supply of allochthonous food sources, i.e. availability of drift-kelp, is often suggested as a proximate trigger of change in sea urchin grazing behaviour, yet field tests of this hypothesis are rare. Here we conduct a suite of in situ behavioural surveys and manipulative experiments within kelp beds and on urchin barrens to examine foraging movements and evidence for a behavioural switch to an overgrazing mode by the Australian sea urchin Heliocidaris erythrogramma (Echinometridae). Tracking of urchins using time-lapse photography revealed urchin foraging to broadly conform to a random-walk-model within both kelp beds and on barren grounds, while at the individual level there was a tendency towards local ‘homing’ to proximate crevices. However, consistent with locally observed ‘mobile feeding fronts’ that can develop at the barrens-kelp interface, urchins were experimentally inducible to show directional movement toward newly available kelp. Furthermore, field assays revealed urchin grazing rates to be high on both simulated drift-kelp and attached kelp thalli on barren grounds, however drift-kelp but not attached kelp was consumed at high rates within kelp beds. Time-lapse tracking of urchin foraging before/ after the controlled addition of drift-kelp on barrens revealed a reduction in foraging movement across the reef surface when drift-kelp was captured. Collectively results indicate that the availability of drift-kelp is a pivotal trigger in determining urchin feeding modes, which is demonstrably passive and cryptic in the presence of a ready supply of drift-kelp. Recovery of kelp beds therefore appears possible if a sustained influx of drift-kelp was to inundate urchin barrens, particularly on reefs where local urchin densities and where grazing pressure is close to the threshold enabling kelp bed recovery.

Lineage

The study was carried out in the semi-enclosed coastal environment of Port Phillip Bay (PPB) in SE Australia, where H. erythrogramma is the most influential herbivore on shallow rocky reefs and demonstrates both ‘passive’ (feeding on drift-kelp) and active (feeding on attached seaweeds) forms of foraging. To assess urchin foraging dynamics, 4 different experiments were conducted across 4 regions of PPB. The regions represented a gradient in urchin overgrazing impacts from relatively small barrens patches of 10-100s m2 within kelp beds typical of southern regions, to extensive ‘continuous’ barrens stretching over 100,000s m2 of sub-tidal reef in northern and western regions. In the north, kelp beds predominantly feature Ecklonia radiata, with only sparse growth of fucoid species (Sargassum spp. and Cystophora spp.) whereas in the southern regions kelp beds show more fucoid algae and a more developed understory. The underlying reef substratum was consistent across all regions, occurring as mixed boulder / flat rock reef interspersed by sand patches to a depth of 5.5 m.

Directional movement of urchins towards attached kelp
Experimental design: This ‘choice’ experiment was conducted in April 2014 in the north of PPB on barrens habitat (depth range 3 – 4 m). Single urchins, situated on the top of large flat boulders, were randomly chosen for use in the trials. Six dive weights were placed equidistantly at a radius of 200 mm around each selected urchin taking care not to disturb the urchins. The dive weights alternatingly held down pieces of kelp (E. radiata) and surrogate kelp (brown cloth) folded in half in such a way that the two free ends faced the urchin. The cloth surrogate was similar in structure, colour and size to the E. radiata pieces. The dive weights were coated in epoxy and both the weights and surrogate cloth were preconditioned on the sea floor for 2 months prior to start of the experiment to mitigate potentially negative effects of any unknown leachates. Hydrodynamic conditions were monitored with an additional dive weight holding a light piece of plastic tape 10cm in length which was position just within the field of view of the camera. During all trials water movement was slightly tidal, this means that there was low movement towards the shore and from shore.
To differentiate urchin choice between natural vs surrogate kelp, the trials were monitored with time-lapse photography. A camera (Panasonic Lumix DCM TS4 in underwater housing) was placed on a 1 to 1.5 m tall tripod fixed to the benthos with tie-downs, and set to take still shots of the trial every 15 mins over a 15 hour period (pilot trials indicated that a time-lapse frequency of 15 mins sufficiently captured the slow urchin movement dynamics). The period of 15 hours was chosen to ensure that the choice the urchin made was captured with the camera During trial set-up, individual urchins were neither touched nor moved. A total of 11 replicate trials on different urchin individuals were conducted, all of which were started at midday. A ‘choice’ was recorded when the urchin moved to the kelp or to the surrogate and stayed at that position for more than 30 min (2 consecutive time-lapse images) or alternatively moved entirely out of the field of view, at which point the trial was deemed to have resulted in ‘nil choice’.

Movement rates of urchins in different regions and habitats
Experimental design: Movement of H. erythrogramma was assessed periodically using time-lapse photography from summer 2012 to summer 2014 in the western, northern and southeastern regions of PPB. To monitor movement of urchins, 4 time-lapse cameras were used as described above. In this experiment, the frequency of photographs was every 5 minutes and each sequence was 5 hours in duration (i.e. 60 images in total). This was done to adequately capture changes in direction and speed of individual urchins. These sequences were taken in each region, in kelp and barrens habitat if both habitats were present. Six replicate time-lapse sequences were taken in each habitat and in each region during the 2 years (2012 – 2014, n = 30 sequences). Each sequence was photographed on a unique patch of reef containing unique urchin individuals to maintain independence of replicate sequences. Criteria for identifying suitable locations in barrens and kelp habitat were that the reef had low topographic relief with high densities of urchins able to be squarely framed within the camera’s field of view. For each image sequence, an object of known dimensions was photographed to enable calibrating the dimensions of the field of view. Preliminary trials were run at night in the north and southeast in barrens habitat to assess movement across the entire diel cycle. Trials conducted during the day and night (4 replicates for the night and 5 for the day period; n = 9) revealed no significant difference of movement between day and night for the different regions. For photographing at night the flash of the cameral was used, this was considered to have little effect on the urchins. All subsequent monitoring of urchins was therefore performed during daylight hours, which increased ease of camera deployments and retrievals.

Kelp consumption rates in different habitats
Experimental design: A standardised assay of sea urchin herbivory was used to compare rates and types of feeding behaviour of urchins on different types of kelp food sources on barrens and in kelp beds, across the 4 different regions of PPB during March 2014. Following the protocol of Vanderklift and Wernberg (2008), assays in kelp and barrens habitats in the same region occurred at a minimum separation distance of 50 m, to ensure the urchin populations were independent based on maximum urchin movement rates over the duration of the assay. Prior to the start of the assays, urchin densities/m2 and biomass/m2 were defined for each habitat (Table 2) from a sample of 8 randomly chosen replicate quadrats (1 m2). Densities were converted to biomass by estimating the mean test diameter from n = 10 urchins in each region and habitat, and converting this to biomass based on the relationship between test diameter and weight calculated for each region / habitat (this relationship was determined from 48 – 90 urchins sampled randomly throughout the entire bay). To simulate the different types of kelp food sources (attached kelp on the benthos, drift kelp on the benthos, the canopy of attached kelp elevated away from the substratum, and caged kelp as a control) pieces of kelp were tethered to metal chain in different ways. To mimic attached kelp on the benthos accessible to sea urchins (and any other benthic herbivores), kelp pieces were fastened directly to the chain with clothes pegs. For simulation of drift-kelp, light nylon monofilament fishing line was attached to pieces of chain and a piece of kelp was held in place by a clothes peg at the other end of the fishing line. To examine the amount of fish grazing on kelp, pieces of kelp were fastened as per mimicking drift-kelp, but additionally with a float so that the kelp lamina floated at canopy height and was not accessible to urchins. To account for loss of algae due to tissue degradation and erosion (i.e. the ‘control’ treatment), another set of kelp pieces were fastened directly to the chain and protected with small plastic cages of mesh size 5 mm. Given the short duration of the experiment it was assumed that the lightweight cages did not affect the area of the kelp pieces within them. Each treatment had 12 replicates (48 pieces of algae in total) and the experiment was run for 3 days.
The standardised kelp pieces used in the assays, i.e. 50 mm lengths of clean healthy lateral frond tissue of E. radiata with no visible epiphytes, were freshly harvested on the day of the experiment. To determine kelp loss over the duration of the experiment, the kelp pieces were photographed both prior to and at the conclusion of the assay. Kelp pieces were held flat by pressing the sample between a clear Perspex sheet and an opaque sheet and photographed. The change in kelp area was calculated using the freeware ImageJ as a proxy to estimate rates of consumption (the area of the ‘control’ pieces did not change over the course of the experiment). To convert consumption rates as planar area to biomass, 10 kelp sections ranging in size were taken to the laboratory, photographed and wet weights taken in order to calculate biomass per unit area.

Behavioural response of sea urchins to drift-kelp availability
Experimental design: The change in activity of H. erythrogramma associated with the presence / absence of drift-kelp was monitored using time-lapse photography. The experiment was implemented as a before-after control-impact (BACI) design, whereby urchin movement within a total of eight plots of ~ 0.6 m2 on barrens habitat was monitored before and after the addition of drift-kelp to treatment plots (n = 4) alongside control plots (n = 4) to which no drift-kelp was added. The experiment was conducted during October 2014, with the BACI design involving an initial 4 hours of tracking before the drift-kelp treatment was added and then a subsequent 4 hours of tracking following the application of kelp. The treatment involved gently placing drift-kelp against all sea urchins within the field of view of the camera and within a 0.5 m buffer zone surrounding the camera field of view. Upon detection of the drift-kelp (a fresh cut lateral of E. radiata) urchins invariably extended their tube feet and seized the piece, which typically took on the order of 10 seconds.

Created: 2019-03-18

Data time period: 2012-08-23 to 2014-04-25

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