Big Backyard Bloom: The Domoic Acid Event of the Decade in Monterey Bay

By Zachary Epperson, MLML Environmental Biotechnology Lab

ECOHAB crew members Zachary Epperson and Steven Loiacono get ready to deploy the new MLML CTD rosette. Photo credit: Dr. Jason Smith.

Over the past few weeks, several marine mammals, particularly sea lions, have been exhibiting some haunting symptoms: writhing on the beach, bending back their necks, or lying suspiciously motionless. As the NOAA-NCCOS-funded, collaborative (MLML, UCSC, MBARI, USC, SCCWRP, UCLA, and IOOS) Ecology & Oceanography of Harmful Algal Blooms (ECOHAB) project gears up for its third week of sampling, data-armed scientists are ready with an explanation—toxic algae. Along with an armada of robotic labs and water quality surveillance vehicles roaming the bay, this field effort provides higher temporal and spatial resolution than our weekly shore based monitoring, which detected initiation of a mixed species Pseudo-nitzschia bloom in April (http://oceandatacenter.ucsc.edu/PhytoBlog/).

The diatom Pseudo-nitzschia spp. is known to produce the neurotoxin domoic acid (DA), responsible for cases of domoic acid poisoning (DAP, also known as amnesic shellfish poisoning), when contaminated tissue is consumed in high enough quantities. Symptoms of DAP may include vomiting, diarrhea, abdominal cramps, headache and dizziness; in severe cases the victim may experience difficulty breathing, confusion, disorientation, seizures, permanent loss of short‑term memory, coma and death. For this reason, recreational harvesting of shellfish is usually quarantined from about late April to Halloween.

A light microscope slide from a phytoplankton tow containing Pseudo-nitzschia chains. Photo credit: USCS-Kudela Lab.
A light microscope slide from a phytoplankton tow containing Pseudo-nitzschia chains. Photo credit: USCS-Kudela Lab.

Though a spring bloom of Pseudo-nitzschia is typical, what’s surprising this year is the total DA load. According to Dr. Raphe Kudela (UCSC) levels this high haven’t been seen since the year 2000! And ECOHAB is out there to track it.

So what is MLML doing specifically, and what does this DA event mean for local marine life (and our clam chowder)? Over the past two weeks, MLML’s Environmental Biotechnology Laboratory (EBL), in collaboration with UCSC and USC research teams, has been sampling twice a week in Monterey Bay from the R/V John H. Martin (MLML). Each day, water is sampled at multiple stations using MLML’s new conductivity, temperature, and depth (CTD) rosette profiler. Water samples are taken from depths of interest, which is then processed and analyzed on board and back at the lab. By making these measurements and data sets, researchers hope to elucidate bloom and toxin dynamics and processes. One recently constructed product of this research, made by the Central and Northern California Ocean Observing System (CENCOOS), is an interactive and predictive model for Pseudo-nitzschia blooms and DA production, which can be accessed online (http://www.cencoos.org/data/models/habs). As a MLML student, it’s been fascinating to see the practicality of our coursework in this research. Classes like Biological and Chemical Oceanography draw immediate connections to the concepts and sampling methods used in this study. Due to the irregularity of a bloom this toxic, it’s also been interesting to see how multiple research teams snap into action, processing samples all week and weekend, and collaboratively discussing and tracking the bloom’s behavior and dynamics. What’s more, the timing of our ECOHAB cruise this spring is nothing short of impeccable; we’ve been able to track this bloom virtually from it’s beginning with incredible resolution!

ECOHAB crew members Dr. Jason Smith, Kendra Negrey, Alyssa Gellene, and Jayme Smith extract a water sample from the rosette for phytoplankton incubation experiments. Photo Credit: Zachary Epperson.
ECOHAB crew members Dr. Jason Smith, Kendra Negrey, Alyssa Gellene, and Jayme Smith extract a water sample from the rosette for phytoplankton incubation experiments. Photo Credit: Zachary Epperson.

As regards our seafood diet, DA tissue levels in shellfish, particularly mussels, are unsafe for recreational harvesting and consumption (note that commercially harvested shellfish are only sold after passing food safety standards, and can be trusted.) A rockfish tissue sample collected from Stillwater Cove showed detectable levels of DA, as have Monterey Bay squid, but these do not currently pose a human health threat being below the regulatory limit of 20 ppm (μg DA/g tissue).  In terms of the ecosystem, DA has been detected throughout the food web and will likely have biomagnifying effects, especially if the bloom continues and DA levels remain high.

In the end, more samples need to be taken to better capture the effect of this massive event. EBL will be conducting zooplankton tows during our final cruises to assess DA levels in primary consumers and hopes to collect sand crab samples from Monterey beaches (san crabs have been collected from the MBARI-MLML Norte beach with toxic DA tissue loads.)  Of course, a key interest is the piscine and piscivorous food webs. Benthic fishes, especially flatfish are needed to assess the ecosystem. If anyone is interested, EBL will gladly accept any specimens from local divers or fisherman. Whole body is best, but not required. A sample’s date caught and location would also be appreciated. We are located across from small boats in the Norte facility (7544 Sandholdt Rd, Rm 36). We’ll be accepting specimens over the next few weeks.

Tales from the Field in Antarctica: Post 3

By Jamie Sibley Yin

Dr. Valerie Loeb is an adjunct professor at Moss Landing Marine Labs. Currently, she functions as an independent Antarctic ecosystem research scientist collaborating with Jarrod Santora of UC Santa Cruz. In April, she headed out to sea with a new NSF funded project entitled "Pilot Study:   Addition of Biological Sampling to Drake Passage Transits of the 'LM Gould'".  The following are updates from the field by Jamie Sibley Yin who is in charge of communications.

 

April 19th, 2015 - Palmer Station and Ice Fish Project

A view of the Lawrence M. Gould (our ship) and Palmer Station.
A view of the Lawrence M. Gould (our ship) and Palmer Station.

When I woke up it was hard to believe we were in the same ocean as last night.  The water was glassy and glaciers cut with snow-capped black rock towered on either side of us.  We were due at Palmer Station in less than an hour.  Palmer was the final destination for some folks—but not us.  We were going with the ship, wherever she went.

This meant fishing in Gerlache Strait and recovering underwater gliders from Shackleton Ridge.

Palmer far exceeded my expectations for a station on an island off the coast of Antarctica.  It’s nestled between light blue glaciers and looks out to the rock-studded ocean.  The station feels like a ski cabin, fire roaring in thewood stove and floor to ceiling glass windows.  The facilities are excellent and include a sauna and outdoor hot tub.  After lunch we walked up the glacier behind the station (think gentle sloping glacier—nothing hard core).  We take a radio and write our estimated time of arrival on the board.  If you are not back by this time, the rescue team at Palmer must spring into action and come find you.  The Antarctic landscape is harsh and far from any medical facilities, thus, every precaution is taken to prevent and minimize injuries.

A large seal near the station.
A large seal near the station.

After our glacier jaunt, dinner was served at the station, everyone from the ship was invited to dine with the station dwellers.  All was merry and the food was spectacular: tacos with chile verde, seared fish, heaping bowls of guacamole and honeydew relish.  Who knew food could be so wonderful in Antarctica.

I was a bit sad to leave station after basking in its’ glory for only two days, but to sea again it was.  This leg of the journey was for the icefish group to catch their fish.  They are studying two groups of fish: Nototheniods, an endemic group of Antarctic fish, and Channichthids, also known as icefish.  Icefish are unique in that they don’t have hemoglobin, a vital oxygen-binding protein found in the blood of all vertebrates.  Their blood is therefore milky white.  They are studying the thermo-tolerances of these fish and how they will respond to warmer water temperatures, potentially modeling their response to climate change.

A gravid icefish in the lab at Palmer Station.
A gravid icefish in the lab at Palmer Station.

They have a lab set up at the station but first they must find their fish.  They use pot traps and benthic trawls to fish.  The boat goes to specific locations where they have had success catching their fish in previous years.  The trawling areas must have sandy bottoms (so the net doesn’t become snagged on underwater pinnacles).  The pots are deployed in strings of four.  They are left out for 24 hours after which we retrieve them and the fish inside.  The icefish are strange-looking creatures, with flat elegant mouths and large sentient eyes they look more like crocodiles than fish.

Kristin, one of the PIs of the icefish project getting ready to unload a fish.
Kristin, one of the PIs of the icefish project getting ready to unload a fish.

 

 

Our zooplankton sampling has been put on hold until the fish crew is done.  We are still sorting through our samples and attempting to identify all our critters, including some very small copepods that are barely a few millimeters in length.  It will be interesting to see how their composition changes when we sample closer to the continent.

Tales from the Field in Antarctica: Post 2

By Jamie Sibley Yin

Dr. Valerie Loeb is an adjunct professor at Moss Landing Marine Labs. Currently, she functions as an independent Antarctic ecosystem research scientist collaborating with Jarrod Santora of UC Santa Cruz. In April, she headed out to sea with a new NSF funded project entitled "Pilot Study:   Addition of Biological Sampling to Drake Passage Transits of the 'LM Gould'".  The following are updates from the field by Jamie Sibley Yin who is in charge of communications.

 

April 9th, 2015 - Northern Drake Passage

Checking out one of the critters with the microscope.
Checking out one of the critters with the microscope.

Our first net tow scheduled for 2am was cancelled.  I breathed a sigh of relief.  I was nervous about sorting and identifying species of zooplankton I had never seen before, staying up late into the night, and working with no end in sight.

The tow didn’t actually get cancelled, but got pushed back to 9am.  We eventually dropped our net in the water at 11am. The net we use is called a Isaacs Kidd Midwater Trawl and is a vast swath of tough black nylon suspended by cord that hangs from a large metal hook.  The whole contraption looks like an off-kilter puppet.  The marine technicians are the ones that actually deploy our nets.  It’s time.  The ship slows to a crawl, the net slithers off the back deck into the icy waters.  Half an hour later the cod end is delivered to us in a bucket.  The cod end is a thick white plastic container with mesh holes.  It’s attached at the end of the net and the unfortunate critters that don’t swim away are trapped there.   The sample is a pink wriggling gelatinous blob.  We dump it into another container and add seawater.  Copepods, krill, amphiphods buzz around the dish, relieved to be in salty water once again.  The salps, jelly fish, and chaetognaths are already dead.  We pick them out with tweezers and count them.  After sorting, counting, and recording all organisms in the sample except for the tiny copepods we are done.  The stations were we sample are five hours apart going full speed on the boat.  We have one hour to recuperate before the next station.

The marine technicians pulling in our net, an Isaacs Kidd Midwater.
The marine technicians pulling in our net, an Isaacs Kidd Midwater.

We sampled six of the nine stations planned for the southbound transit.  It was a brutal two days as we processed samples around the clock, catching two, maybe three hours of sleep when we could.  I was not enthusiastic about missing my precious sleep, but the night samples were filled with loads of small shiny fish, called myctophids, which were so cool I soon forgot my lack of sleep.

The ship journey overall was quite calm except for our very last day in transit.  Waves pummeled the side of the boat and splashed my window on the third floor, snow flew sideways outside, it was difficult to even stand without bracing myself against a wall.  My productivity on the ship fell to zero as I all my focus turned to just functioning. Peering through a microscope and trying to sort krill is no easy task when the water in your petri dish sloshes from side to side every time the boat goes through a wave.  Books and DVDs hurled themselves from the shelves in the lounge.  People slid off the leather couches as the boat continued to rock.  It felt like a fun house—one that was not so fun and that you couldn’t leave.

Tales from the Field in Antarctica: Post 1

By Jamie Sibley Yin

Dr. Valerie Loeb is an adjunct professor at Moss Landing Marine Labs. Currently, she functions as an independent Antarctic ecosystem research scientist collaborating with Jarrod Santora of UC Santa Cruz. In April, she headed out to sea with a new NSF funded project entitled "Pilot Study:   Addition of Biological Sampling to Drake Passage Transits of the 'LM Gould'".  The following are updates from the field by Jamie Sibley Yin who is in charge of communications.

 

April 8th, 2015 - First Entry

My chair sways gently, a jackhammer-like sound comes from an undisclosed location, men with white beards and black wire rimmed glasses stare into their laptops.  Where am I? I’m somewhere in the Straits of Magellan, en route to Antarctica.

Hi, my name’s Jamie and I’m going to share my journey to, and my time in Antarctica with you all.  I’m a recent marine biology graduate from the University of California, Santa Cruz, and I’m working with Valerie Loeb of Moss Landing Marine Labs on her ecosystem survey of Drakes Passage.

Today was the first day of real work--which I have been eagerly anticipating.  It wasn’t quite what I was expecting but, then again, I haven’t known what to expect this whole time.  There was lots of back and forth, running in and out of the ship. Tying down the microscopes and lights putting away boxes of petri dishes, pipettes, and one liter glass jars.

Outside the cool wind blows and the sea delivers unexpected blasts of seawater to my face.  It’s cold, but not unbearably so.  We have been issued special ECW (extreme cold weather) gear, which consists of everything you need to survive on an Antarctic boat including steel-toed boots (always needed on deck) and lined rubber gloves similar to the ones my mother uses to wash dishes.

The bird and marine mammal observer for our project, Mike, said he saw a minke whale and various birds including a giant petrel.  I visited him in the bridge where he does his observations behind panoramic windows through a large pair of binoculars.  The bridge is on the fourth level of the ship where the captain and mates orchestrate the movement of our ship, the Lawrence M. Gould or LMG.  All I could spot were some birds that looked like small sea gulls (actually Antarctic fulmars), and lots of choppy waves.  On the horizon I saw a snowy island, which, upon further inspection proved to be a cruise ship.

I’m still getting my “sea legs” as they say, and after breakfast I felt like regurgitating the eggs and bacon I had just eagerly consumed.  But after seeing a whale, some  Peale’s dolphins, and two penguins, my on-the-verge seasickness had left me.  It was time to take a nap in preparation for our 2am zooplankton net tows.

Jamie standing in front of the US's National Science Foundation's icebreaker and research vessel, the Laurence M. Gould, named after an American scientist.
Jamie standing in front of the US's National Science Foundation's icebreaker and research vessel, the Laurence M. Gould, named after an American scientist.

Project summary by Dr. Valerie Loeb

Overview

Changes in the Southern Ocean due to climate warming are expected to be visible in ecosystem dynamics.  Analysis of ADCP records from supply transits of Drake Passage by the “L.M. Gould”, 1999-present, indicate that underway observations of the upper ocean scattering layer can serve as a proxy to monitor these changes.  Recent results indicate that interannual variability in backscattering strength (i.e., quantity of responsible organisms) is correlated to climate indices.  The interpretation of these ecological changes is severely limited because the sound scatterers have not been identified and linkages to upper trophic level predators are unknown.  This project adds biological sampling to the “L.M. Gould” time series with the expectation that ADCP data, calibrated with net-tow data and depth-referenced underwater videography and predator distribution, can be used to extend the spatio-temporal coverage of in situ sampling in Drake Passage.

Intellectual Merit

This proposal provides a novel approach on how to make use of long term ADCP records in identifying those organisms responsible for seasonal, interannual and longer term variability observed in ADCP records collected since 1999.  Net tows accompanied by videography during spring, autumn and winter periods will provide information on the abundance and taxonomic-size composition of organisms likely to be dominant sound scatterers within the 3 biogeographic zones of Drake Passage.  The distribution and densities of distinct zooplankton assemblages and backscattering strength will be linked to seabird/mammal predator populations to illuminate ecologically important areas (i.e., characterized by high trophic transfer), which may be candidates for Important Bird Areas (BirdLife International). Establishment of “bottom-up” trophic connections enable future integrated assessments of climate variability on upper trophic level predators.  Examination of ADCP backscatter variability and trends in southern Drake Passage with respect to zooplankton data independently collected here from 1994-2009 should indicate organisms underlying past ADCP trends and cycles relative climate indices (e.g., ENSO). Successful implementation of this project may initiate spatially and temporally coherent biological sampling extending over a sufficient number of years into the future that would provide statistically robust data sets on the species composition and abundance of zooplankton and seabird/mammal populations essential for assessment of significant ecosystem change in Drake Passage associated with a warming Southern Ocean.

Our first field season is October 27-November 22, 2014 (Austral spring) and the second is in April-May, 2015 (autumn).

To the End of the Earth (for Kelp!)

By Heather Kramp, Ichthyology Lab

Chile is dotted with volcanoes, and we
Puerto Montt is surrounded by farmland, volcanoes, and fjords, with the Andes looming the distance, making for amazing views on our flights in and out. Photo: Heather Fulton-Bennett

In early January of this year, I boarded a plane bound for Puerto Montt, Chile. It was my first time to South America and my first time crossing the equator. Though Chile is an amazing vacation destination, I was headed there for an even better purpose - research! Myself and five other MLML graduate students were fortunate to have the opportunity to take a ten-day intensive field course at the Universidad de Los Lagos in Puerto Montt. The course, Global Kelp Ecosystems, is taught every three years in partnership with MLML and the Universidad de Los Lagos. Five instructors co-teach the course, including Drs. Michael Graham and Scott Hamilton of MLML, Dr. Alejandro Bushman from the Universidad de Los Lagos, and Drs. Silvain Faugeron and Alejandro Pérez-Matus from the Pontifica Universidad Católica de Chile. In addition to MLML students, four Chilean graduate students and one French graduate student studying in Chile also took the course.

The 2015 Global Kelp Systems class in Pucatrihue, Chile
The 2015 Global Kelp Systems class in Pucatrihue, Chile.

After a day-and-a-half of travel with an unbelievable amount of luggage (including dive gear) we all arrived in Chile.

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Ichthyology, the R/V Point Sur, and McDonalds

By Stephen Pang

There are few times that I would willingly wake up while it is still dark outside. The day of our ichthyology field trip aboard the R/V Point Sur was one of those days. Not only would it be my first time aboard the Point Sur, it would also be my last before its retirement after 28 years of service at Moss Landing Marine Labs. Suffice to say, I was pretty excited to have this opportunity.

The R/V Point Sur

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MLML goes to Baja – the trip continues

 By Jackie Lindsey, Vertebrate Ecology Lab

For the next two weeks Moss Landing Marine Labs will be a little quieter, and not just because of spring break.  A large class of graduate students has just departed for Baja California Sur for two weeks of field research, and I am lucky to be among them!   Many of us have never been to this part the world, and we are full of hopes and dreams that we can pull off the projects we designed back in the classroom.

El Pardito
El Pardito

We are spending the majority of our trip on a tiny island called El Pardito, located within the Sea of Cortez.  This island is home to a small community of fishermen who have lived on the island for generations.  Many of us are depending heavily on their expertise to set up our projects and navigate the local waters.

Our projects range from mapping benthic habitat, to monitoring Marine Protected Areas, to studies of sea turtles and damselfish. We are spending full days in and on the water around El Pardito, and the weather should be just about perfect (fingers crossed)!

When we get back there will be plenty of pictures to post, commemorating our journey and all our hard work, but for now let me leave you with this image of NOT EVEN ALL OF THE GEAR!  Food, cooking tools, boats, compressors, dive gear, camping gear, sampling gear...the list goes on and on (and on and on).

Sampling gear
Sampling gear
Dive gear explosion
Dive gear explosion

I hope we didn't forget anything because it's too late now!  See you in two weeks!

Bon Voyage Baja Class!

By Kristin Walovich

IMG_1245The Marine Operations Building (aka the Firehouse) has been a busy place this morning. The Marine Environmental Studies of the Gulf of California class is staring their journey toward La Paz, Mexico today, eventually landing on a small island called Isla Partida just north of La Paz. Here they will conduct a variety of field research projects including sea floor mapping, fish grazing and artisanal fishing studies as well as fish, seaweed and invertebrate surveys.  Check back in a few weeks for a more detailed account of their adventures!

IMG_1230
Graduate students Dorota Szuta and Devona Yates check dive gear before loading their equipment into one of three vehicles traveling down to Baja California.
Captain Jon Douglas (JD) helps Scott Miller and Evan Mattiasen add a bit of extra space to the boat trailer for more gear.
Captain John Douglas (JD) helps Scott Miller and Evan Mattiasen add a bit of extra space to the boat trailer for more gear.
IMG_1243
Dissecting scope, first aid kit, generator, boat patch kit, FOOD, inflatable boats for diving, transect tapes...the list of supplies seems endless for this 3 week endeavor.
IMG_1256
Clint Collins lashes gear to the roof while Instructor Scott Hamilton and Ashley Wheeler load to food supplies.

Nitrox and Boat Dives – Wrapping Up MLML’s Fall Science Diving Course

By Heather Fulton-Bennett, Phycology Lab

MLML's fall AAUS Science Diving course is coming to an end, and what better way finish than with a pair of boat dives from our own R/V John Martin.

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The R/V John H. Martin from a diver's view (Photo: Scott Gabara)

As part of the course, students get certified in Nitrox diving, a gas mix with a higher percentage of oxygen than normal air. This mix allows for longer bottom times and decreased surface intervals, which is a huge advantage for conducting research underwater.

Last week we were lucky enough to have our last dives of the semester in Carmel Bay, at Pescadero Wash Rock and outer Copper Roof House.

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Kathryn along the Wash Rock wall (Photo: Diana Steller)
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Marissa and Lindsay examine turf algae and benthic invertebrates (Photo: Scott Gabara)
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Thanks to all who made it an amazing semester!

Sea otters participate in coastal restoration

by Jackie Lindsey, Vertebrate Ecology Lab

There's a new reason to love the world's smallest marine mammal species - so let's talk sea otters!

These voracious predators are again making headlines in the science world as a new paper comes hot off the (virtual) presses.  Hughes et al. (2013) published an article in PNAS entitled "Recovery of a top predator mediates negative eutrophic effects on seagrass".  This paper is truly a local collaboration, with scientists from UCSC's Long Marine Lab, the Elkhorn Slough reserve, USGS, CSU Monterey Bay, and MBARI.

The headline? Sea otters may have saved the Elkhorn Slough seagrass habitat by doing what they do so well: eating crabs.

Photo credit: Ron Eby http://www.vcstar.com/photos/2013/aug/26/307245/
Photo credit: Ron Eby http://www.vcstar.com/photos/2013/aug/26/307245/

To fully understand the premise of the paper, here's a little ecology review:

When we think about the health of a marine ecosystem, we often think of two major ways that the system could be controlled.

1) Top down:  A classic example of top down control is sea otters consuming urchins in a kelp forest.  These three trophic levels depend heavily on one another, so that if the sea otters in the kelp forest are removed by a predator (humans or killer whales) and can no longer keep the sea urchin population in check, the urchins will become overpopulated and consume so much of their prey (the kelp) that the kelp disappears, taking with it other creatures in the ecosystem that depend upon it.  If the sea otters are returned to the system, they consume enough sea urchins that the kelp is released from predation pressure, and the ecosystem can return to normal balanced levels.  Here's a figure by Estes et al. (1998) to illustrate this classic example.  Focus on the cartoons and the arrow sizes to track who eats what in each scenario.

Estes et al. 1998
Figure 1 from Estes et al. 1998

2) Bottom up: Think of bottom up control like the workings of a traditional garden.  If you over-fertilize your tomato plants and they start to die off as a result, this bottom up forcing will impact the aphids that depend on the tomato plant for food, and in turn their ladybug predators.

Ladybugs consuming aphids on a tomato plant http://extension.umd.edu/growit/photos-aphids
Ladybugs consuming aphids on a tomato plant http://extension.umd.edu/growit/photos-aphids

Was that example not "marine" enough for you?  Let's get back to the sea otter news!

It is well known that Elkhorn Slough, an estuary located right next to MLML, is a nutrient-loaded system due to nearby agricultural activity.  In the past, biologists noticed that nutrient loading was having a negative impact on the estuarine reserve's seagrass beds, when algal epiphytes bloomed and overtook the seagrass.  (That's bottom up control!)  Hughes et al. showed that in the last 30 years, that trend of declining seagrass beds was reversed, even as agricultural runoff increased!

How??  Hughes et al. noticed that another thing happened about 30 years ago: southern sea otter populations recovered to the point that otters began colonizing Elkhorn Slough habitats.  Was this a coincidence?  The authors think that this is an example of an interaction between top down and bottom up control.

Figure 2a from Hughes et al 2013
Figure 2a from Hughes et al. 2013

Hughes et al. (2013) demonstrated that the interaction between sea otters and their prey species in Elkhorn slough created a 4-level trophic cascade that released the seagrass from top down control pressures, allowing it to flourish even in the presence of high nutrient loads.  In short, the sea otters ate the crabs, which in turn consumed less algal epiphyte grazers (snails, slugs), which in turn consumed more algal epiphytes (blanketing the seagrass), which allowed the seagrass to grow. This well-timed trophic cascade was lucky for the seagrass, and all other marine critters that depend on it for habitat in Elkhorn Slough.

The sea otters are helping to restore our coastline, and you can too!  Just five days until California's Coastal Cleanup Day, and it's not to late to volunteer!

My citations, in case you want to do a little more reading,:

Brent B. Hughes, Ron Eby, Eric Van Dyke, M. Tim Tinker, Corina I. Marks, Kenneth S. Johnson, and Kerstin Wasson (2013) Recovery of a top predator mediates negative eutrophic effects on seagrass. PNAS: 1302805110v1-201302805.

Estes JA, Tinker MT, Williams TM, Doak DF (1998) Killer whale predation on sea otters linking oceanic and nearshore ecosystems. Science 282(5388): 473-476