Reef flat in front of the UC Berkeley Gump Station, Cook's Bay, Mo'orea, French Polynesia
Research Overview
Whether it is through photosynthesis, chewing on plants, or actively capturing dinner, gaining energy from the environment is essential for any organism on Earth. Predation, in particular, is an exciting avenue for research because the relationship between predators and their prey is so integral to the evolution of morphology and ecology. I am particularly excited about predation in marine invertebrates. While invertebrates make up the majority of marine biodiversity, they are often overlooked as important contributors to food webs
My most recent work aims to uncover the key macroinvertebrate predators on coral reefs. Occupying less than one percent of the sea floor, coral reefs are home to more than twenty-five percent of all marine life, most of which live inside the many tunnels and crevices that make up the coral reef matrix. It is therefore highly likely that key invertebrate predators on coral reefs remain to be discovered.
Thus, I am collaborating with coral reef ecologists and engineers in robotics and computer science to address the central question:
what is the biodiversity and environment like inside the coral reef matrix?
My work on the role of macroinvertebrates on coral reefs is grounded in the relationship between feeding morphology and ecology. A foundational tenet in animal ecology is that species with specialized feeding morphologies consume very specific prey types. The powerful seed-crushing beak of a Galapagos finch and the long nectar-sucking proboscis of a hawkmoth provide classic examples of the tight link between feeding morphology and ecology. Understanding the diet-morphology relationship has provided valuable insights into the ecological and evolutionary processes that shape the vast morphological diversity seen across organisms and that underlie community structure.
My research suggests, however, that highly specialized feeding morphology does not necessarily correspond to diet specialization. Instead, animals considered to be specialists consume a wider range of prey than would be predicted based on their morphology alone.
I use tools from physiology, biomechanics, behavior, food web ecology, and stable isotope ecology to answer the question:
how, when, and why does specialized morphology either limit or enhance diet breadth?
Given the importance of abiotic factors in shaping these relationships, another main goal of my research is to understand
how environmental disturbances, such as ocean acidification and ocean warming, can disrupt links between diet and morphology.
Biodiversity & Environment
Investigating a hole inside the reef matrix using a GoPro on a selfie stick and a pH and temperature sensor attached to a data logger (SeaFET inside the gear bag) in a coral reef of West Maui, Hawaii.
What is life like inside the coral reef matrix?
Coral reefs are among the most diverse ecosystems in the world. Despite the incredible biodiversity that has already been documented, true coral reef diversity remains largely a mystery, because current technology has limited the study of reefs to only their outer surfaces. Coral reefs are massive, three-dimensional structures with many tunnels and crevices that make up the coral reef framework. The majority of species living within reefs and the biological, ecological, and chemical processes that sustain these unique ecosystems remain undiscovered, simply because it has been impossible to access internal reef structures non-destructively.
Exploring inside coral reefs is becoming more imperative as anthropogenic threats to the ocean, such as climate change, pollution, and overfishing, drive the disappearance of healthy reefs worldwide. Ocean acidification (OA) is of particular concern. The acidity of the world’s oceans is increasing at an unprecedented rate, which is dramatically changing ocean ecosystems. OA profoundly alters the hard structures of many calcifying marine organisms, including ecologically important species of corals. Yet, the question of how entire reef ecosystems respond to OA remains largely unresolved because researchers are limited in their abilities to evaluate how OA will affect the internal reef structure. This information is critical because it will help determine how reefs may cope with and potentially adapt to future OA conditions.
In an effort to understand the processes that sustain coral reefs, I have begun a new project collaborating with the The Sandin Lab, a coral reef ecology lab at Scripps Institution of Oceanography, Bioinspired Robotics and Design Lab, a soft robotics lab in Mechanical and Aerospace Engineering. We aim to turn the reef “inside out” to answer two basic questions: 1) who lives inside coral reefs and 2) what is the environment like there. Answers to these questions will reveal currently undiscovered organisms as well as critical information about the environment that sustains these diverse ecosystems.
Ecology
Mantis shrimp feeding ecology: you are what you eat
The key to testing ecological and evolutionary correlations between morphological and diet specialization rests on accurately describing appendage functional morphology and reconstructing diet over a range of spatial and temporal scales.
To accurately quantify diet, I established the use of stable isotope analysis (SIA) in mantis shrimp. Determining how food incorporates into body tissues is essential for using SIA to analyze diet. In collaboration with an undergraduate student, two eco-physiologists, and a disease ecologist, I experimentally determined isotopic incorporation rates (time required for the diet to assimilate into different tissues) and discrimination factors (difference between the predator and prey isotopes) of carbon and nitrogen in a smasher. I compared these results to a range of taxa and found that the carbon incorporation rates were consistent with an allometric relationship in aquatic ectotherms, suggesting a correlation between body size and incorporation rate across aquatic animals (deVries, Martínez del Rio, Tunstall, and Dawson. 2015. PLOS ONE).
Neogonodactylus bredini smashing a snail. (Photo: Roy L. Caldwell)
With assistance from five undergraduate students, and in collaboration with a graduate student, a behavioral ecologist, a plant ecologist, and an ecophysiologist, I employed SIA coupled with a laboratory feeding experiment and field studies of prey abundance to analyze diet in the reef flat smasher, Neogonodactylus bredini. Using Bayesian methods to determine the proportional contributions of each prey to the diet, I found that, counter to expectation, smashing appendages allow N. bredini to consume both hard- and soft-bodied prey, thereby broadening diet breadth (deVries, Stock, Christy, Goldsmith, Dawson. 2016. Oecologia). Thus, mantis shrimp may be important links between reef flat macro-invertebrates and larger, mobile animals because mantis shrimp consume many different prey and are also consumed by a diversity of larger predators.
To lay the foundation for exploring comparative questions of form and function across mantis shrimp, I compared the diet breath of two small smasher and spearer species that co-occur in coral rubble in Mo'orea, French Polynesia. Surprisingly, I found that the spearer has a wider diet breadth than the smasher, suggesting that both of these species consume hard-shelled prey but the spearer is more adept at capturing evasive prey (deVries. 2016. Biology Letters).
Morphology
Strike mechanics and behavior of a spearing mantis shrimp
Many spearer are ambush predators that hunt for prey from a burrow that they build in the sand. The goal of for all ambush predators is to quickly minimize the distance between themselves and their prey. Ambushing prey in water is particularly difficult because of the added challenges to moving imposed by the density and viscosity of water.
To establish a baseline mechanical comparison between spearers and smashers, I performed the first biomechanical and kinematic analysis of spearing in collaboration with a former undergraduate student (E. Murphy - Univ. California, Berkeley [UCB]) and a biomechanist (Dr. S. Patek - Duke University). Using high-speed and field videos of prey capture events, we determined the kinematics and mechanics of the spearing strike in one small spearer species, Alachosquilla vicina (body length 24-27 mm), and one large species, Lysiosquillina maculata (body length 130-170 mm).
Lysiosquillina sulcata spearing a fish. (Photo: Roy L. Caldwell)
We found that the strike of the small species, A. vicina, was much faster (5.2 m/s in 3.3 ms) than that of the large species, L. maculata (2.3 m/s in 34 ms) because A. vicina appears to generate spring-loaded strikes, while L. maculata does not. Both species, however, exhibited greater reach but lower speeds and accelerations compared to previous research on smashers (14-23 m/s in 2.7 ms; Patek et al. 2004. Nature). This key finding indicates that while spearers move fast enough to capture evasive prey, they cannot generate the accelerations and forces required for smashing hard-shelled prey. Spearing strike speeds and durations, however, were on the order of other aquatic ambush predators, such as garter snakes, suction feeding wrasse, and squid tentacles.
Is smashing always a success? How a smashing mantis shrimp consumes both hard-shelled and soft-bodied prey.
I learned from my work on the smashing mantis shrimp, Neogonodactylus bredini that this species of smashing mantis shrimp uses a repertoire of behaviors to consume different prey. In collaboration with a biomechanist (J. R. A. Taylor - Scripps Institution of Oceanography) and three undergraduate students, I am working to examine the feeding behaviors that N. bredini uses to consume hard-shelled clams and evasive grass shrimp in detail using high-speed videos of prey capture events. I have found that the strikes used to break clams are much faster than those used to capture grass shrimp. N. bredini also grabs grass shrimp with its maxillipeds, suggesting that it does not rely solely on its powerful strikes to capture prey.
Environmental effects on mantis shrimp exoskeleton and mechanics
Former undergraduate mentee, Summer Webb, collecting data on the hardness and stiffness of the mantis shrimp exoskeleton using a nanoindentor materials testing machine. (Photo: Emily L. A. Kelly)
Given the importance of abiotic factors in shaping diet-morphology relationships, another main goal of my research is to understand how environmental disturbances can alter links between diet and morphology. Thus, I have investigated the potential impacts of climate change stressors, namely ocean acidification (OA) and ocean warming, could directly impact feeding mechanics and diet in N. bredini by modifying the integrity of the smashing appendage.
With collaborators in physiology, biomechanics, and engineering, and assistance from six undergraduate students, I exposed N. bredini individuals to the pCO2 and temperature values projected for the year 2100 years. From, indicators of oxidative stress to the ultrastructure, mineral content, and material properties of the appendage exoskeleton, N. bredini showed no significant responses to treatment conditions. These results indicate that, unlike other intertidal organisms, N. bredini tolerates an expanded range of pH and temperature without experiencing oxidative stress or changes to the exoskeleton, thereby leaving the integrity of the predatory appendage intact. Thus, mantis shrimp may be able to exploit less tolerant species under future ocean conditions because many of their hard-shelled prey are predicted to have thinner shells that will be easier to break.
* Undergraduate or recent undergraduate mentee.
To begin to understand how mantis shrimp cope with simulated OA and OW, I am collaborating with a graduate student at SIO to determine the genetic underpinnings of N. bredini’s wide tolerance range using transcriptomics. Preliminary analyses suggest that myosin, a key structural component of muscles, exhibits differential expression between treatments, suggesting that OA adversely affects muscle physiology.
Additionally, I am currently collaborating with two recent undergraduate students, a biomechanist, and a physiologist, to examine whether the combined stress of OA and low food conditions yield measureable changes in feeding behavior, muscle physiology, and exoskeleton mineralization.