Lillian J. Tuttle Raz

I wish to integrate research in basic ecology with applied management and conservation. I am fascinated by the behavioral and physiological mechanisms by which species interact with each other and with their rapidly changing environments. Equipped with this mechanistic understanding, I can better measure and predict the effects of local stressors (e.g., introduced species, coastal development, and overfishing) on biological populations and communities. I work in the field and lab using a combination of observational and manipulative experiments.

Below are my most recent lines of inquiry:

developing coral-reef management tools

Ecosystem-based management (EBM) must rely on strong science, and yet it is often challenging to bridge the gap between the worlds of research, resource use, and policy. My current work aims to provide management programs with the information and tools they need to implement EBM, place-based planning, pono fishing practices, and effective monitoring and restoration efforts.

To that end, I am orchestrating multiple systematic literature reviews that will identify how interacting stressors impact coral health, recruitment, and survival. My colleagues and I have integrated this information into a meta-analytical framework that identifies management thresholds for sediment (deposited and suspended), nutrients, and contaminants on nearshore coral-reef ecosystems. This project is in association with NOAA’s Pacific Islands Regional Office whose essential fish habitat consultation process “provides recommendations to federal agencies to avoid, minimize, mitigate, or otherwise offset the effects of their actions” on coral reefs in the Pacific region.  

Relevant Publications:

Tuttle and Donahue (2022) and (2020 - NOAA Technical Report) detail the results of a systematic review and meta-analysis of the effects of deposited and suspended sediment on corals. It follows the methods described in Tuttle et al. (2020).

Nalley, Tuttle, et al. (2021) is a systematic review and meta-analysis that derives water quality thresholds for common coastal pollutants that damage corals. We compiled a global dataset addressing the effects of metals, pesticides, PAHs, PCBs, and pharmaceuticals on coral health. For data-rich contaminants, we used hierarchical Bayesian models to describe dose-response curves between concentration and metrics of coral health.

Tuttle et al. (2020) is a methodology paper that describes the protocol for conducting a systematic review and meta-analysis of the effects of sedimentation and turbidity on reef-building coral species. It is the basis for subsequent systematic reviews for other common co-stressors, including nutrient enrichment, contaminants/pollutants, light attenuation, and freshwater discharge.

Ingeman et al. (2017) clarifies seemingly conflicting advice to managers of Caribbean coral reefs affected by the Indo-Pacific red lionfish, a recent invasive predator.

planktonic predator-prey interactions

How do microscopic animals interact in the ocean? Marine plankton are important as the basis of complex food webs and fisheries, and yet we lack a mechanistic understanding of their behaviors and population dynamics. This "black box" thereby limits our ability to predict the vulnerability of plankton to climate change and ocean acidification.

My colleagues and I document and quantify the development of both predatory attack behavior and prey evasion, and how these affect the outcomes of predator-prey interactions in a clownfish-calanoid copepod model system. From the prey's perspective, we investigate the roles that evasion capabilities of different developmental states and different species of copepods have on susceptibility to a fish predator. From the predator's perspective, we study the development of attack strategies and kinematics during the fish's early life (first two weeks post-hatching). 

Relevant Publications:

(1) Tuttle et al. (2019) revealed that copepods sense minuscule water movements within the bow wave of its predator, much smaller in magnitude than previously thought. This weak signal triggered escape jumps away from the predator, despite the additional challenge of detecting the predator’s direction.

(2) Fashingbauer, Tuttle et al. (2019) describes a highly modified and previously undescribed fast-start of larval clownfish, which can capture highly evasive prey as early as one day after hatching.

IMPORTANCE & VULNERABILITY OF MUTUALISMS

As voracious, generalist predators of fishes, invasive lionfish may eat and/or alter the behavior of cleaning gobies (Elacatinus spp.): ubiquitous, conspicuous, and ecologically important species that clean parasites off of other reef fishes. If lionfish do affect cleaning gobies, then cleaning mutualisms among native species could be weakened, leading to increased transmission of parasites on invaded reefs. I conducted a combination of field and lab experiments to test if lionfish (1) eat the cleaner goby (E. genie), (2) learn not to eat the cleaner goby that have a putative skin toxin, and/or (3) indirectly affect the growth and persistence of cleaner goby recruits on small coral patch reefs.

Relevant Publications:

(1) Tuttle (2017) was a before-after-control-impact field experiment that found no direct or indirect effect of invasive lionfish on the native cleaner goby. However, lionfish did reduce populations of another cleaner, the juvenile bluehead wrasse. Lionfish may have also indirectly caused fewer large predators to aggregate around patch reefs. This surprising result may impact recreational, commercial, and subsistence fisheries in the region that target large predatory fishes.

(2) Tuttle et al. (2015 and 2021) found that captive lionfish will eat the cleaner goby but quickly learn not to. This learned aversion is the likely result of a previously undescribed chemical defense on the skin of the goby, which caused lionfish to hyperventilate.

role of parasites in marine ecoSYSTEMS

Successful invasions are largely explained by some combination of enemy release, where the invader escapes its natural enemies from its native range, and low biotic resistance, where native species in the invaded range fail to control the invader. I examined the extent to which parasites may mediate both release and resistance in the introduction of lionfish to Atlantic coral reefs.

Relevant Publications (first-author and co-authored):

(1) Sikkel et al. (2014) found that lionfish are weakly susceptible to one type of generalist ectoparasite, the gnathiid isopod, in both the native Pacific and introduced Atlantic ranges.

(2) Ramos-Ascherl et al. (2015) was a survey of macroparasites infecting lionfish in the Cayman Islands, The Bahamas, and Puerto Rico.

(3) Consistent with patterns of both enemy release and low biotic resistance, Tuttle et al. (2017) found that invasive lionfish had much lower rates of infection by parasites than native Pacific lionfish and ecologically similar native Atlantic fishes. 

Behavior as a window into evolution

My previous postdoc investigated the evolutionary mechanisms that generate novel, adaptive function in animals. Along with other members of the cavefish lab at UH-Manoa, I used the Mexican tetra as a model organism. In addition to cavefish losing their eyes and pigment, cavefish are behaviorally distinct from their surface-dwelling brethren. For example, cavefish do not sleep, and have lost certain cooperative behaviors, such as schooling, and competitive behaviors, such as aggression. Thanks to the incredibly simple environments in which these cavefish evolved (sparse food and no light or predators), we can more easily isolate the effects of "nature versus nurture" on the unique development, physiology, and behaviors of these fish. I conducted several behavioral assays, and helped integrate these results with those of hybrid analyses and Next-Gen sequencing to resolve our questions of how these animals interact with each other and their environment.

Relevant Publications (co-author):

(1) Yoshizawa et al. (2018) discovered surprising behavioral similarities between cavefish and humans with autism spectrum disorder. There are many orthologs for autism-risk genes in cavefish that are up- or down-regulated in the same way as humans, and which experience more positive selection than other genes across the cavefish/human genome. Autism-like behaviors in cavefish were also mitigated by pharmaceuticals used for autism patients, further supporting the idea that these behaviors are the result of similar neural pathways in cavefish and autism patients.

(2) Worsham et al. (2019) is a paper and video that shares our freeware-based methods for studying cavefish behavior and physiology.