Ten best practices for effective phenological research.

The number and diversity of phenological studies has increased rapidly in recent years. Innovative experiments, field studies, citizen science projects, and analyses of newly available historical data are contributing insights that advance our understanding of ecological and evolutionary responses to the environment, particularly climate change. However, many phenological data sets have peculiarities that are not immediately obvious and can lead to mistakes in analyses and interpretation of results. This paper aims to help researchers, especially those new to the field of phenology, understand challenges and practices that are crucial for effective studies. For example, researchers may fail to account for sampling biases in phenological data, struggle to choose or design a volunteer data collection strategy that adequately fits their project's needs, or combine data sets in inappropriate ways. We describe ten best practices for designing studies of plant and animal phenology, evaluating data quality, and analyzing data. Practices include accounting for common biases in data, using effective citizen or community science methods, and employing appropriate data when investigating phenological mismatches. We present these best practices to help researchers entering the field take full advantage of the wealth of available data and approaches to advance our understanding of phenology and its implications for ecology.

Decadal-scale phenology and seasonal climate drivers of migratory baleen whales in a rapidly warming marine ecosystem.

Species' response to rapid climate change can be measured through shifts in timing of recurring biological events, known as phenology. The Gulf of Maine is one of the most rapidly warming regions of the ocean, and thus an ideal system to study phenological and biological responses to climate change. A better understanding of climate-induced changes in phenology is needed to effectively and adaptively manage human-wildlife conflicts. Using data from a 20+ year marine mammal observation program, we tested the hypothesis that the phenology of large whale habitat use in Cape Cod Bay has changed and is related to regional-scale shifts in the thermal onset of spring. We used a multi-season occupancy model to measure phenological shifts and evaluate trends in the date of peak habitat use for North Atlantic right (Eubalaena glacialis), humpback (Megaptera novaeangliae), and fin (Balaenoptera physalus) whales. The date of peak habitat use shifted by +18.1 days (0.90 days/year) for right whales and +19.1 days (0.96 days/year) for humpback whales. We then evaluated interannual variability in peak habitat use relative to thermal spring transition dates (STD), and hypothesized that right whales, as planktivorous specialist feeders, would exhibit a stronger response to thermal phenology than fin and humpback whales, which are more generalist piscivorous feeders. There was a significant negative effect of western region STD on right whale habitat use, and a significant positive effect of eastern region STD on fin whale habitat use indicating differential responses to spatial seasonal conditions. Protections for threatened and endangered whales have been designed to align with expected phenology of habitat use. Our results show that whales are becoming mismatched with static seasonal management measures through shifts in their timing of habitat use, and they suggest that effective management strategies may need to alter protections as species adapt to climate change.

Climate change effects on biodiversity, ecosystems, ecosystem services, and natural resource management in the United States.

Climate change is a pervasive and growing global threat to biodiversity and ecosystems. Here, we present the most up-to-date assessment of climate change impacts on biodiversity, ecosystems, and ecosystem services in the U.S. and implications for natural resource management. We draw from the 4th National Climate Assessment to summarize observed and projected changes to ecosystems and biodiversity, explore linkages to important ecosystem services, and discuss associated challenges and opportunities for natural resource management. We find that species are responding to climate change through changes in morphology and behavior, phenology, and geographic range shifts, and these changes are mediated by plastic and evolutionary responses. Responses by species and populations, combined with direct effects of climate change on ecosystems (including more extreme events), are resulting in widespread changes in productivity, species interactions, vulnerability to biological invasions, and other emergent properties. Collectively, these impacts alter the benefits and services that natural ecosystems can provide to society. Although not all impacts are negative, even positive changes can require costly societal adjustments. Natural resource managers need proactive, flexible adaptation strategies that consider historical and future outlooks to minimize costs over the long term. Many organizations are beginning to explore these approaches, but implementation is not yet prevalent or systematic across the nation.

It's about time: A synthesis of changing phenology in the Gulf of Maine ecosystem.

The timing of recurring biological and seasonal environmental events is changing on a global scale relative to temperature and other climate drivers. This study considers the Gulf of Maine ecosystem, a region of high social and ecological importance in the Northwest Atlantic Ocean and synthesizes current knowledge of (a) key seasonal processes, patterns, and events; (b) direct evidence for shifts in timing; (c) implications of phenological responses for linked ecological-human systems; and (d) potential phenology-focused adaptation strategies and actions. Twenty studies demonstrated shifts in timing of regional marine organisms and seasonal environmental events. The most common response was earlier timing, observed in spring onset, spring and winter hydrology, zooplankton abundance, occurrence of several larval fishes, and diadromous fish migrations. Later timing was documented for fall onset, reproduction and fledging in Atlantic puffins, spring and fall phytoplankton blooms, and occurrence of additional larval fishes. Changes in event duration generally increased and were detected in zooplankton peak abundance, early life history periods of macro-invertebrates, and lobster fishery landings. Reduced duration was observed in winter-spring ice-affected stream flows. Two studies projected phenological changes, both finding diapause duration would decrease in zooplankton under future climate scenarios. Phenological responses were species-specific and varied depending on the environmental driver, spatial, and temporal scales evaluated. Overall, a wide range of baseline phenology and relevant modeling studies exist, yet surprisingly few document long-term shifts. Results reveal a need for increased emphasis on phenological shifts in the Gulf of Maine and identify opportunities for future research and consideration of phenological changes in adaptation efforts.

Trophic influences on mercury accumulation in top pelagic predators from offshore New England waters of the northwest Atlantic Ocean.

Trophic pathways and size-based bioaccumulation rates of total mercury were evaluated among recreationally caught albacore tuna (Thunnus alalunga), yellowfin tuna (Thunnus albacares), shortfin mako shark (Isurus oxyrinchus), thresher shark (Alopias vulpinus), and dolphinfish (Coryphaena hippurus) from offshore southern New England waters of the northwest Atlantic Ocean between 2008 and 2011. Mercury concentrations were highest in mako (2.65 ± 1.16 ppm) and thresher sharks (0.87 ± 0.71 ppm), and significantly lower in teleosts (albacore, 0.45 ± 0.14 ppm; yellowfin, 0.32 ± 0.09 ppm; dolphinfish, 0.20 ± 0.17 ppm). The relationship between body size and mercury concentration was positive and linear for tunas, and positive and exponential for sharks and dolphinfish. Mercury increased exponentially with δ (15)N values, a proxy for trophic position, across all species. Results demonstrate mercury levels are positively related to size, diet and trophic position in sharks, tunas, and dolphinfish, and the majority of fishes exhibited concentrations greater than the US EPA recommended limit.

Defensive responses of cuttlefish to different teleost predators.

We evaluated cuttlefish (Sepia officinalis) responses to three teleost predators: bluefish (Pomatomus saltatrix), summer flounder (Paralichthys dentatus), and black seabass (Centropristis striata). We hypothesized that the distinct body shapes, swimming behaviors, and predation tactics exhibited by the three fishes would elicit markedly different antipredator responses by cuttlefish. Over the course of 25 predator-prey behavioral trials, 3 primary and 15 secondary defense behaviors of cuttlefish were shown to predators. In contrast, secondary defenses were not shown during control trials in which predators were absent. With seabass-a benthic, sit-and-pursue predator-cuttlefish used flight and spent more time swimming in the water column than with other predators. With bluefish-an active, pelagic searching predator-cuttlefish remained closely associated with the substrate and relied more on cryptic behaviors. Startle (deimatic) displays were the most frequent secondary defense shown to seabass and bluefish, particularly the Dark eye ring and Deimatic spot displays. We were unable to evaluate secondary defenses by cuttlefish to flounder-a lie-and-wait predator-because flounder did not pursue cuttlefish or make attacks. Nonetheless, cuttlefish used primary defense during flounder trials, alternating between cryptic still and moving behaviors. Overall, our results suggest that cuttlefish may vary their behavior in the presence of different teleost predators: cryptic behaviors may be more important in the presence of active searching predators (e.g., bluefish), while conspicuous movements such as swimming in the water column and startle displays may be more prevalent with relatively sedentary, bottom-associated predators (e.g., seabass).

Species- and size-specific variability of mercury concentrations in four commercially important finfish and their prey from the northwest Atlantic.

Total mercury was analyzed as a function of body length, season, and diet in four commercially and recreationally important marine fish, bluefish (Pomatomus saltatrix), goosefish (Lophius americanus), silver hake (Merluccius bilinearis), and summer flounder (Paralichthys dentatus), collected from continental shelf waters of the northwest Atlantic Ocean. Mercury levels in the dorsal muscle tissue of 115 individuals ranged from 0.006 to 1.217 µg/g (wet weight) and varied significantly among species. The relationship between predator length and mercury concentration was linear for bluefish and summer flounder, while mercury levels increased with size at an exponential rate for silver hake and goosefish. Mercury burdens were the highest overall in bluefish, but increased with size at the greatest rate in silver hake. Seasonal differences were detected for bluefish and goosefish with mercury levels peaking during summer and spring, respectively. Prey mercury burdens and predator foraging habits are discussed as the primary factors influencing mercury accumulation.