I grew up playing along the salt marshes and beaches of coastal South Carolina where I developed an interest in the diversity of animals I 'discovered' throughout my childhood while crabing, shrimping, oystering, and using sea squirts like water guns. I followed this interest as an undergraduate working on scallop restoration and the predictors of suitable habitat in Rhode Island during a summer internship with NOAA and an undergraduate thesis on invasive species in Charleston, South Carolina. Much of my research interest since that time have been driven by these early experiences with a number of projects predicting suitable habitat and understanding how marine organisms colonize novel habitats. Given larvae are the primary dispersive life-history stage in many marine organisms I am particularly interested in the role early life-history stages play in shaping the distributions of species.
Range limits of invasive species
For my PhD with Dr. Amy Moran I examined the distribution and physiology of the barnacle Megabalanus coccopoma to understand its potential range limits within its introduced range in the southeastern US. I surveyed the distribution of M. coccopoma within the southeastern US to compare to my range limit estimates based on adult thermal tolerance, and documented a large range retraction and rapid re-expansion following an extremely cold winter (Crickenberger & Moran 2013). These range shift data were used to test the predictive accuracy of the species distribution model MaxEnt (Crickenberger 2016). MaxEnt and other species distribution models are commonly use to predict range limits of introduced species and consequences of climate variability, but are rarely tested using empirical data. My work suggests the dynamics of range expansion in tropical species may be fundamentally different from temperate species when both are moving poleward because tropical species typically lack the ability to acclimate to high-latitude winter temperatures, which may explain the large range retraction I documented. Another interesting finding was that contrary to work done with temperate species, which suggests larval thermal tolerances often set range limits, long-term exposure of adults to cold temperatures was the best predictor of geographic distribution (Crickenberger et al. 2017). My species distribution models suggested that range-limiting mechanisms can vary spatially, and that correlative species distribution models can predict both range limits of invasive species and the consequences of climate variability.
As an undergraduate I was the first to the non-native mussel Perna viridis in South Carolina (Crikenberger & Sotka 2009). Now that I am living in Hong Kong I have begun a collaboration with Matt Gilg at the University of North Florida to examine differences in cold tolerance between native populations in Hong Kong and non-native populations in Florida. We will use these physiology data to make predictions about the distribution of P. viridis and compare these predictions to those from correlative species distribution models.
Front cover of local newspaper following my discovery of Megabalanus coccopoma and Perna viridis in Charleston Harbor.
Local adaptation of marine larvae
Another focus of my PhD work examined how crustacean larvae are adapted to regional climate regimes, and the effects of physiological adaptation on population connectivity. More specifically, I examined local adaptation of thermal tolerance windows of larvae of the tropical barnacle Pollicipes elegans. P. elegans is only found in northern Mexico, El Salvador, and Peru and is absent in the equatorial region between these areas where water temperatures are warmer. Along with complementary genetic analyses that found low gene flow among these three populations, this work suggests larvae from these three populations are locally adapted to the thermal regimes they experience, and warm equatorial water temperatures may limit dispersal into, but not out of El Salvador (Walther et al. 2013). In the two populations where temperatures vary with the seasons, Mexico and Peru, we examined the thermal acclimatization capacity of larvae (Crickenberger et al. 2015). We found larvae from one region were able to acclimatize to seasonal changes in temperature, but larvae from another could not. We proposed that these population-level differences in acclimatization capacity may be related to recent thermal history, low selection for acclimatization due to irregular patterns of seasonal temperature change during El Niño events, or to different phylogeographic histories of Northern- and Southern-hemisphere populations. Further work by our collaborators on the timing of divergence of these three populations and patterns of paternity can be found in these publications (Plough & Marko 2013, Plough et al. 2014, Marchant et al. 2015).
Changes in distribution due to climate change
During my postdoc with Dr. David Wethey we studied the mechanisms responsible for driving the distribution of the barnacle Semibalanus balanoides hundreds of kilometers north on both sides of the Atlantic Ocean over the past century. We found reproductive failure likely drove the range retraction of S. balanoides in Europe, but not in the USA. Reproductive failure is likely driven by mortality during brooding and not energy limitation of embryos during prolonged or warm brooding conditions (Crickenberger, McAlister, & Wethey, in prep). In the USA survival of new recruits is likely more important in setting the southern range limit than the effects of temperature on early life-history stages because fertilization, brooding, and the probability of larval release matching phytoplankton availability were all predicted to be high near the historical range edge. Phytoplankton mismatch was predicted to be much more likely in the Gulf of Maine in the USA and the English Channel and Galicia in Europe which may partially explain the ephemeral patterns of recruitment in these regions (Crickenberger & Wethey 2017).
After developing these models we were lucky enough to test them by monitoring recruitment patterns during the warmest year on record since 1870 and a cooler than average year near the southern range limit of S. balanoides along the US coastline. Our models incorporated the impacts of temperature on brooding, fertilization, competency dependent larval dispersal and adult density as a metric for larval pool to provide nearly perfect predictions of biogeographic patterns of field recruitment. Furthermore, our models of reproductive success suggested interior range collapse may be an important, and under-appreciated, mechanism driving long-term range dynamics of benthic marine invertebrates. Another interesting finding from the competency dependent dispersal models is that we found no evidence of changes in patterns of connectivity between years despite differences in temperature during the dispersal period, when larvae were growing. Based on monitored quadrats of freshly settled recruits within the historical range juvenile survival was likely the primary driver of the historical range retraction, however, reproductive failure may lead to further range collapse in the future based on our model predictions and surveys of reproductive success during the warmest reproductive season since 1870, the earliest date of our temperature dataset. Very few studies incorporate these types of mechanistic models into biogeographic predictions and even fewer have found evidence to suggest mechanisms of range limitation can change through time (Crickenberger & Wethey 2018).
During my surveys of S. balanoides I also measured patterns of abundance and recruitment of Chthamalus stellatus which colonized the northeastern US towards the end of the 19th century. In collaboration with John Wares and others we combined historical distribution data, recent surveys of recruitment and abundance, metapopulation modeling, and population genetics to understand its colonization history. Interestingly, we found natural colonization of the northeastern US was likely driven by warming temperatures during this time period (Wares et al., submitted). We also have some limited data suggesting C. stellatus may be able out compete S. balanoides near the southern range limit of S. balanoides due to high level of Chthamalus recruitment and low levels of Sembalanus recruitment (S. Crickenberger, unpublished data).
Interactions between sexual selection, climate change, and behavior
In my current postdoc with Dr. Gray Williams I am working on several different projects using snails within the family Neritidae as a model system. In one set of projects we are testing whether sexual selection and natural selection (i.e. temperature) select for size in the same or different directions. Thermal tolerance is not size dependent in Nerita yoldii. However, we did find both veligers in egg capsules in the intertidal and adults have very narrow thermal safety margins, and that without behavior all adults would die due to exposure to lethal temperatures (Chan et al., in prep). More experiments are currently underway to examine the importance of behavior in preventing mortality in N. yoldii and how the importance of behavior in preventing mortality may vary along the coastline of China. We are also generally exploring the importance of thermoregulatory behavior in intertidal ectotherms (Crickenberger et al., in prep). Preliminary experiments on mate choice in the field and trail following in the lab suggest males are not choosing to mate with females significantly larger than those found by random chance (Crickenberger et al., in prep) and we have not found any evidence of sex-dependent trail following. Experiments are underway to look at cryptic female choice using microsatellite markers.
We are beginning a project to test the climate variability hypothesis using the 8-10 species of snails in the family Neritidae found in Hong Kong and any other neritid species we can get our hands on. Using heart beat rates we are interested in both the breadth of thermal tolerance relative to range size and body temperature variance in addition to the slope of the warmer portion of the performance curve. Much of our understanding about the susceptibility of tropical species to climate change is based on assumptions about thermal tolerance breath and the slope of performance decline at warmer temperatures, however, limited empirical tests exist particularly for marine organisms. The goal of this project is to test these assumptions using a primarily tropical family of snails, Neritidae.