Romi L. Burks

Cued in: Advances and opportunities in freshwater chemical ecology

We focus this mini-review on how naturally occurring chemical cues mediate ecological interactions, especially interspecific competition and predation in freshwater communities. Although freshwater chemical ecology lags behind terrestrial and marine chemical ecology, we identify recent progress toward: (1) identifying the chemical composition of cues important in food web interactions, e.g., specific glucosinolates, benzyl succinoates, and lignoids as deterrents to herbivory on freshwater macrophytes; (2) employing a nonreductionist approach that tests for emergent responses to suites of multiple chemical cues, e.g., trade-offs in snail refuge-seeking behavior in the presence of chemical cues from both fish and crayfish; (3) investigating how abiotic forces, such as hydrodynamics, impact chemical communication across a broad spatial and temporal scale, e.g., drift responses of mayfly nymphs to whole-stream additions of trout cue; and (4) quantifying the importance of genetic variability, e.g., how chemical cues change selective pressures of local environments. The questions of interest in freshwater chemical ecology cross taxonomic boundaries; traverse broad spatial and temporal scales; demonstrate nonlinear, unpredictable results; and necessitate a multidisciplinary approach for adequate understanding.

Insights from an Integrated View of the Biology of Apple Snails (Caenogastropoda: Ampullariidae)

ABSTRACT Apple snails (Ampullariidae) are among the largest and most ecologically important freshwater snails. The introduction of multiple species has reinvigorated the field and spurred a burgeoning body of research since the early 1990s, particularly regarding two species introduced to Asian wetlands and elsewhere, where they have become serious agricultural pests. This review places these recent advances in the context of previous work, across diverse fields ranging from phylogenetics and biogeography through ecology and developmental biology, and the more applied areas of environmental health and human disease. The review does not deal with the role of ampullariids as pests, nor their control and management, as this has been substantially reviewed elsewhere. Despite this large and diverse body of research, significant gaps in knowledge of these important snails remain, particularly in a comparative framework. The great majority of the work to date concerns a single species, Pomacea canaliculata, which we see as having the potential to become a model organism in a wide range of fields. However, additional comparative data are essential for understanding this diverse and potentially informative group. With the rapid advances in genomic technologies, many questions, seemingly intractable two decades ago, can be addressed, and ampullariids will provide valuable insights to our understanding across diverse fields in integrative biology.

Center Stage: The Crucial Role of Macrophytes in Regulating Trophic Interactions in Shallow Lake Wetlands

Hydrophilic, or water-loving, macrophytes characterize wetland ecosystems, indicating prerequisite conditions of hydric soils and sufficient hydrology. The presence of such macrophytes is a key descriptor in multiple wetland def- initions (Lewis 2001a) and macrophytes may be further used to actually describe particular types of wetlands, such as cattail marshes. Macrophytes contribute significant biomass to wetland systems and represent a critical component of wetland biogeochemistry as primary producers and drivers of organic matter cycling within aquatic systems. In this chapter, we argue that macrophytes occupy the center of trophic interactions in shallow lakes, influ- encing outcomes through structural, behavioral and chemical interactions. We define shallow lakes as permanently flooded wetlands that often contain submerged or floating macrophytes and that may be surrounded by emergent vegetation (i.e.marshy habitat). Shallow remains a relative term in limnology circles, but typically is less than 3 m average depth, such that macrophytes can fill a substantial portion of the water column and stratification is neither pre- dictable nor long-term. Such systems may be termed lakes, ponds or wetlands, depending on their size and the ecological context. Macrophytes may regulate trophic interactions in ephemeral systems without permanent inundation.

Pelagic prey and benthic predators: impact of odonate predation on Daphnia

Interactions between benthic predators and pelagic prey, such as larval odonates and Daphnia, are often used to describe classic predator–prey relationships in laboratory studies. However, few field studies explore the potential impact of benthic predators on pelagic prey. Recent studies of cladocerans document diel horizontal migration (DHM), where large-bodied zooplankton (i.e., Daphnia) decrease their exposure to pelagic predators by seeking refuge among macrophytes. However, daphnids undergoing DHM may simultaneously increase their likelihood of encountering benthic predators that commonly occur in littoral zones. In laboratory experiments, we showed that dragonfly nymphs (Epitheca cynosura) effectively eliminated all Daphnia within 24 h, regardless of macrophyte presence or architecture. We also tested whether additions of larval damselflies (Ischnura elegans, Coenagrion puella, C. pulchellum) and dragonflies (Somatochlora flavomaculata) (total odonate density of 35–55/m2) significantly reduced total zooplankton or benthic invertebrate abundance in field enclosures with different macrophyte densities (20, 40, 80% volume infested [PVI]). Odonates significantly reduced Daphnia abundance at 20 PVI. However, the magnitude of the influence of odonates on daphnids, as well as Ceriodaphnia and Polyphemus, decreased with increasing macrophyte density. Odonate predation did not significantly affect benthic taxa abundance. Thus, daphnids undergoing DHM may lower predation from pelagic predators, but our results suggest that mortality from littoral predators may be significant. The net benefit of DHM may, therefore, differ among lakes as a function of the relative threats posed by pelagic and littoral predators.

Colonial aggregates: effects of spatial position on zebra mussel responses to vertical gradients in interstitial water quality

Vertical gradients in interstitial water quality may develop within densely organized assemblages of sessile aquatic organisms. These gradients may compromise the survival of individuals. We examined whether a vertical gradient of interstitial water chemistry (NO3-N, NH4-N, and dissolved oxygen [DO]) would develop within dense zebra mussel (Dreissena polymorpha) colonies in a laboratory flume (flow rate ∼1 cm/s). Over a 4-h duration, we found that NO3-N concentrations increased, DO decreased, and NH4-N concentrations remained the same from the surface to the base of 6-cm thick zebra mussel colonies. These results were supported by trends found in natural Lake Michigan zebra mussel colonies at 4 to 6 m depths, where NO3-N concentrations at the base of colonies measured 162% of NO3-N concentrations in open water above the colonies. We also examined how vertical water-quality gradients influenced zebra mussel movement and mortality by tracking the vertical position and survivorship of individual zebra mussels in colonies. Substantial movement out of the base of the colony occurred after 7 and 30 d of incubation. After 30 d, 69% of smaller-sized mussels (≤6 mm) moved upward within the colony from the base, in contrast to 0% movement of larger mussels (>20 mm), whose motility may have been impeded. After 30 d, mortality of all size classes significantly increased, with >50% mortality occurring in the bottom layer. Our studies suggest that dense colonies produce vertical interstitial water-quality gradients at low flow, and that movement out of the base of the colony by smaller mussels may be an important mechanism for survival in dense colonies.

Fecundity of the exotic applesnail, Pomacea insularum

Abstract International trade frequently moves mollusks around the globe, thereby increasing their opportunity to cause ecological and economic damage. Recent genetic studies have confirmed the identity of South American applesnails (Pomacea insularum) in the southeastern US, but limited literature exists on this species. Understanding fecundity provides direct insight into the invasive potential of mollusks. Our study documents P. insularum fecundity in Texas and offers comparisons with the closely related global invader P. canaliculata. We quantified P. insularum clutch and hatchling physical characteristics and examined field and laboratory hatching success. Clutches contained thousands of eggs (mean = 2064 eggs), and clutch size tended to increase over the reproductive season. Clutches exhibited average field and laboratory hatching efficiencies (number of hatchlings/total number of eggs) near 70 and 30%, respectively. Notably, several clutches hatched at 80% or higher in the field. Exotic P. insularum deposit more eggs/clutch than the related invader P. canaliculata, but we do not yet know how seasonal hatching efficiencies compare. However, even with a conservative estimate of 1 to 10% survival to adulthood, the average P. insularum clutch yields 14 to 144 new applesnails. The high fecundity of P. insularum translates into considerable ecological impact because adult females can contribute >1 clutch/wk over an extended growing season in the southeastern US. The need for research has increased with the emergence of P. insularum populations in the fragile Florida Everglades. We advocate life-history studies like ours to help understand the invasion potential of applesnails and other invasive mollusks.

Comparing applesnails with oranges: the need to standardize measuring techniques when studying Pomacea

Although invaders come in all shapes and sizes, several mollusks have recently achieved notoriety as both economically and ecologically costly invaders. Applesnails of the genus Pomacea get their name from reaching the size of an apple. Native to South America, the species P. insularum has recently established reproducing, and potentially invasive, populations in Texas, Alabama, Georgia, and Florida. In contrast to the widely invasive golden applesnail (P. canaliculata), few studies of the channeled species P. insularum exist. In studying similar invasive applesnail species, scientists use several methods of measurement. We have explored the relationships among shell height, operculum width, and weight among juvenile and adult P. insularum and tested their inter-measurer reliability. We also investigated the use of shell height, shell length, and operculum width measurements in P. canaliculata studies and observed whether or not those studies defined their measurements. We found that operculum width served as a significantly more reliable measure among researchers. Furthermore, operculum width better predicted weight than shell height. The majority of articles that measured P. canaliculata did not define their measurements, which may cause problems when comparing studies between native and exotic populations or when comparing the two species. We recommend that future studies of P. insularum use operculum width to measure snails and explore a possible sex dimorphism in the operculum width of adult P. insularum.

Pink eggs and snails: field oviposition patterns of an invasive snail, Pomacea insularum , indicate a preference for an invasive macrophyte

Oviposition of non-calcareous or thinly shelled eggs represents an important life stage of many insects, amphibians, and several gastropods. A recently identified invasive species of apple snail, Pomacea insularum, exhibits alarming invasive characteristics of high reproductive rates and generalist consumption patterns. This snail takes the opposite approach to egg laying compared to most aquatic insects as adult snails crawl out of the water to place clutches on emergent, or terrestrial, substrates. As fecundity best indicates invasive potential for mollusks, control or management efforts need to understand reproductive behavior in P. insularum to predict, and hopefully impede, its spread throughout the Gulf Coast of the United States. Specific characteristics of wetlands and shallow lakes may facilitate the invasion process of P. insularum by providing females with conditions that permit successful oviposition. In order to investigate this possibility, we studied P. insularum oviposition behavior in an invasive population at two times during the reproductive season in Texas, USA. Based on a subsequent survey (August 2009), plants comprised 78% of the available habitat. Wild taro (Colocasia esculenta) and alligator weed (Alternanthera philoxeroides) represented 48 and 43% of that proportion, respectively. During 2008–2009, no new concrete or metal structures appeared in our sampling reach and consistent amounts of plant stands and woody debris remained dominant. Given this distribution, P. insularum laid disproportionately more clutches on wild taro compared to its availability and less on alligator weed and bulrush (Schoenoplectus californicus) than expected. Owing to limited metal and concrete substrates, we found a higher proportion of clutches on these artificial substrates than expected in both May and August 2008. However, artificial substrates comprised less than 2% of available substrates in the bayou. Our results suggest that wetlands and shallow lakes surrounded by large emergent macrophytes, particularly wild taro, likely provide ideal oviposition sites for P. insularum, promote egg supply, and possibly facilitate invasion into new aquatic ecosystems.

Count your eggs before they invade: identifying and quantifying egg clutches of two invasive apple snail species (Pomacea).

Winning the war against invasive species requires early detection of invasions. Compared to terrestrial invaders, aquatic species often thrive undetected under water and do not garner notice until too late for early action. However, fortunately for managers, apple snails (Family Ampullariidae, Genus Pomacea) provide their own conspicuous sign of invasion in the form of vibrantly colored egg clutches. Managers can potentially use egg clutches laid in the riparian zone as a means of early detection and species identification. To facilitate such efforts, we quantified differences in characteristics (length, width, depth, mass, egg number) of field-laid clutches for the two most common invasive species of apple snail, P. canaliculata and P. maculata, in native and non-native populations. Pomacea canaliculata native and non-native populations differed noticeably only in width. Native P. maculata clutches possessed significantly greater width, mass and eggs numbers compared with native P. canaliculata. Non-native P. maculata clutches significantly exceeded all other populations in all measured characteristics. Consequently, these traits may successfully distinguish between species. Fecundity data also allowed us to develop models that accurately estimated the number of eggs per clutch for each species based on clutch dimensions. We tested one, two and three dimensional models of clutches, including rendering a clutch as either a complete ellipsoid or an ellipsoid intersected by a cylinder to represent the oviposition site. Model comparisons found the product of length and depth, with a different function for each population, best predicted egg number for both species. Comparisons of egg number to clutch volume and mass implied non-native P. canaliculata may be food limited, while non-native P. maculata appeared to produce such enormous clutches by having access to greater nutrients than the native population. With these new tools, researchers and managers can quickly identify, quantify and begin eradication of new non-native apple snail populations.

To Co-Author or Not to Co-Author: How to Write, Publish, and Negotiate Issues of Authorship with Undergraduate Research Students

The rewards associated with publishing with undergraduate students outweigh the challenges. This Teaching Resource emphasizes the value of publishing with undergraduates and may be particularly helpful to incoming faculty who are new to the process of working with students. Beyond simply extolling the virtues of undergraduate research, we examine how such deep learning experiences for students can translate into unique opportunities for the faculty to demonstrate devotion to both teaching and scholarship. Along with highlighting the reasons faculty should consider publishing with undergraduates, we identify the particular challenges that accompany this suggestion and discuss strategies for overcoming them. Our resource includes two decision trees for helping faculty determine whether publishing with undergraduates represents a reasonable and attainable goal and whether an undergraduate has earned authorship. Based on our experience at primarily undergraduate institutions, we provide a list of strategies that may facilitate writing with undergraduates and lead to certain milestones in the careers of both students and faculty.