Publications

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2019
Schlenger, AJ, Libralato S, Ballance LT.  2019.  Temporal variability of primary production explains marine ecosystem structure and function. Ecosystems. 22:331-345.   10.1007/s10021-018-0272-y   AbstractWebsite

Understanding drivers of ecosystem structure and function is a pervasive goal in academic and applied research. We used 24 synthetic ecosystem-level indices derived from trophic models, and independently derived data for Net Primary Productivity, to investigate drivers of ecosystem structure and function for 43 marine ecosystems distributed in all oceans of the world and including coastal, estuaries, mid-ocean islands, open-ocean, coral reef, continental shelf, and upwelling ecosystems. Of these indices, ecosystem Biomass, Primary Production, Respiration, the ratio of Biomass to Total System Throughput (sum of total energy flow into and out of an ecosystem as well as between ecosystem components), the ratio of Production to Biomass, Residence Time (mean time that a unit of energy remains in the ecosystem), Average Trophic Level, and Relative Ascendency (index of organization and complexity of a food web) displayed relationships with measures of Net Primary Productivity (NPP). Across all ecosystems, relationships were stronger with seasonal and interannual variability of NPP as compared to mean NPP. Both measures of temporal variability were combined into multivariate predictive relationships for each ecosystem index, with r(2) values ranging from 0.14 to 0.49 and Akaike's information criteria values from -8.44 to 3.26. Our results indicate that despite large geographic and environmental differences, temporal variability of NPP is strongly linked to the structure and function of marine ecosystems.

2018
Ballance, LT.  2018.  Contributions of photographs to cetacean science. Aquatic Mammals. 44:668-682.   10.1578/am.44.6.2018.668   AbstractWebsite

Over four decades ago, a short paper demonstrated how photographs of free-swimming dolphins could be used to reveal scientific information about cetaceans. That paper, and a few others published during the same time period, illustrated a research technique that has become foundational in the field of marine mammalogy and resulted in a cascade of science. Photographs can be used to identify individuals, providing insights into movements, migrations, site fidelity, school structure and stability, and abundance. Photographs can be used to estimate group size and improve the precision of abundance estimates. Photographs can characterize reproductive output at the population level. Photographs allow for quantification of morphology, yielding insights into classification at a variety of taxonomic levels; and they provide a means to assess the condition and health of individual animals. And photographs can provide insights into behavior. The information photographs convey and their applications to cetacean research are ever-increasing. Ultimately, photographs have provided a high-quality and relatively inexpensive means to increase the knowledge base for most cetacean species in all of the oceans of the world through research conducted by scientists of developed and developing nations, and through citizen science conducted by non-scientists.

Jones, T, Parrish JK, Peterson WT, Bjorkstedt EP, Bond NA, Ballance LT, Bowes V, Hipfner JM, Burgess HK, Dolliver JE, Lindquist K, Lindsey J, Nevins HM, Robertson RR, Roletto J, Wilson L, Joyce T, Harvey J.  2018.  Massive mortality of a planktivorous seabird in response to a marine heatwave. Geophysical Research Letters. 45:3193-3202.   10.1002/2017gl076164   AbstractWebsite

Climate change has exacerbated the occurrence of large-scale sea surface temperature anomalies, or marine heatwaves (MHWs)-extreme phenomena often associated with mass mortality events of marine organisms. Using a combination of citizen science and federal data sets, we investigated the causal mechanisms of the 2014/2015 die-off of Cassin's Auklets (Ptychoramphus aleuticus), a small zooplanktivorous seabird, during the NE Pacific MHW of 2013-2015. Carcass deposition followed an effective reduction in the energy content of mesozooplankton, coincident with the loss of cold-water foraging habitat caused by the intrusion of the NE Pacific MHW into the nearshore environment. Models examining interannual variability in effort-controlled carcass abundance (2001-2014) identified the biomass of lipid-poor zooplankton as the dominant predictor of increased carcass abundance. In 2014, Cassin's Auklets dispersing from colonies in British Columbia likely congregated into a nearshore band of cooler upwelled water and ultimately died from starvation following the shift in zooplankton composition associated with onshore transport of the NE Pacific MHW. For Cassin's Auklets, already in decline due to ocean warming, large-scale and persistent MHWs might represent a global population precipice. Plain Language Summary During the winter of 2014/2015, thousands of Cassin's Auklets, a small seabird that breeds in the NE Pacific, were found dead on beaches from California to British Columbia, Canada. We show that wide-scale starvation was due to a change in food quality associated with warmer ocean temperatures preceding and during the die-off. This research highlights that more frequent and intense ocean warming events may have complex impacts on food webs with population consequences for marine predators, particularly seabirds such as Cassin's Auklets.

Ballance, LT.  2018.  Cetacean Ecology. Encyclopedia of Marine Mammals. ( Wursig B, Kovacs K, Thewissen J, Eds.)., San Diego: Elsevier
2017
Young, H, Nigro K, McCauley DJ, Ballance LT, Oleson EM, Baumann-Pickering S.  2017.  Limited trophic partitioning among sympatric delphinids off a tropical oceanic atoll. Plos One. 12   10.1371/journal.pone.0181526   AbstractWebsite

Understanding trophic relationships among marine predators in remote environments is challenging, but it is critical to understand community structure and dynamics. In this study, we used stable isotope analysis of skin biopsies to compare the isotopic, and thus, trophic niches of three sympatric delphinids in the waters surrounding Palmyra Atoll, in the Central Tropical Pacific: the melon-headed whale (Peponocephala electra), Gray’s spinner dolphin (Stenella longirostris longirostris), and the common bottlenose dolphin (Tursiops truncatus). δ15N values suggested that T. truncatus occupied a significantly higher trophic position than the other two species. δ13C values did not significantly differ between the three delphinds, potentially indicating no spatial partitioning in depth or distance from shore in foraging among species. The dietary niche area—determined by isotopic variance among individuals—of T. truncatus was also over 30% smaller than those of the other species taken at the same place, indicating higher population specialization or lower interindividual variation. For P. electra only, there was some support for intraspecific variation in foraging ecology across years, highlighting the need for temporal information in studying dietary niche. Cumulatively, isotopic evidence revealed surprisingly little evidence for trophic niche partitioning in the delphinid community of Palmyra Atoll compared to other studies. However, resource partitioning may happen via other behavioral mechanisms, or prey abundance or availability may be adequate to allow these three species to coexist without any such partitioning. It is also possible that isotopic signatures are inadequate to detect trophic partitioning in this environment, possibly because isotopes of prey are highly variable or insufficiently resolved to allow for differentiation.

Ruiz-Cooley, RI, Gerrodette T, Fiedler PC, Chivers SJ, Danil K, Ballance LT.  2017.  Temporal variation in pelagic food chain length in response to environmental change. Science Advances. 3   10.1126/sciadv.1701140   AbstractWebsite

Climate variability alters nitrogen cycling, primary productivity, and dissolved oxygen concentration in marine ecosystems. We examined the role of this variability (as measured by six variables) on food chain length (FCL) in the California Current (CC) by reconstructing a time series of amino acid-specific delta N-15 values derived from common dolphins, an apex pelagic predator, and using two FCL proxies. Strong declines in FCL were observed after the 1997-1999 El Nino Southern Oscillation (ENSO) event. Bayesian models revealed longer FCLs under intermediate conditions for surface temperature, chlorophyll concentration, multivariate ENSO index, and total plankton volume but not for hypoxic depth and nitrate concentration. Our results challenge the prevalent paradigm that suggested long-term stability in the food web structure in the CC and, instead, reveal that pelagic food webs respond strongly to disturbances associated with ENSO events, local oceanography, and ongoing changes in climate.

Joyce, TW, Durban JW, Claridge DE, Dunn CA, H.Fearnbach, Parsons KM, Andrews RD, Ballance LT.  2017.  Physiological, morphological, and ecological tradeoffs influence vertical habitat use of deep-diving toothed-whales in the Bahamas. Plos One. 12(10)   10.1371/journal.pone.0185113  
Redfern, JV, Moore TJ, Fiedler PC, deVos A, R.L. Brownell J, Forney KA, Becker EA, Ballance LT.  2017.  Predicting cetacean distributions in data-poor marine ecosystems. Diversity and Distributions. :1-15.   10.1111/ddi.12537  
Hetherington, ED, Olson RJ, Drazen JC, Lennert-Cody CE, Ballance LT, Kaufmann RS, Popp BN.  2017.  Spatial food-web structure in the eastern tropical Pacific Ocean based on compound-specific nitrogen isotope analysis of amino acids. Limnology and Oceanography.   10.1002/lno.10443  
2016
Joyce, TW, Durban JW, Fearnbach H, Claridge D, Ballance LT.  2016.  Use of time-at-temperature data to describe dive behavior in five species of sympatric deep-diving toothed whales. Marine Mammal Science. 32:1044-1071.   10.1111/mms.12323   AbstractWebsite

This paper develops and validates a method of using time-at-temperature (TAT) histograms from satellite transmitter tags to describe the dive activity patterns and approximate depth distributions of five deep-diving toothed whale species in the northern Bahamas. TAT histograms represent a bandwidth-conserving method of recovering a long-term proxy record of dive activity. However, using temperature to interpret TAT on a scale of approximate depths required the complex estimation of TAT histogram bin boundary depths in a dynamic oceanographic region. Here we evaluated the relative performance of four interpolation methods and a global reanalysis data assimilation model in estimating climatological isotherm depth surfaces within our study area. TAT-derived approximate time-at-depth (TAD) distributions aligned closely with directly observed TAD distributions from a smaller sample of depth-recording satellite tags deployed on separate individuals of each species. TAT-derived approximate depth distributions were also consistent with various published accounts for this suite of species. Estimating dive ranges and time budgets are important components of (1) understanding habitat overlap between species, (2) evaluating the potential role of these predators in meso-and bathypelagic ecosystems, and (3) assessing vulnerability and exposure to anthropogenic impacts.

2015
Lyday, SE, Ballance LT, Field DB, Hyrenbach KD.  2015.  Shearwaters as ecosystem indicators: towards fishery-independent metrics of fish abundance in the California Current. Journal of Marine Systems. 146:109-120.
2014
Priddel, D, Carlile N, Portelli D, Kim Y, O'Neill L, Bretagnolle V, Ballance LT, Phillips RA, Pitman RL, Rayner MJ.  2014.  Pelagic distribution of Gould's Petrel (Pterodroma leucoptera): linking shipboard and onshore observations with remote-tracking data. Emu. 114:360-370.   10.1071/mu14021   AbstractWebsite

This study describes and compares the pelagic distribution and migratory patterns of the two subspecies of Gould's Petrel (Pterodroma leucoptera), and contrasts data obtained from tracking birds at sea using geolocators with observational data (shipboard sightings, by-catch records and beachcast specimens). While breeding, tracked individuals of both subspecies (P. l. leucoptera and P. l. caledonica) foraged within the Tasman Sea and south of the Australian continent, with forays west into the Indian Ocean before laying. After breeding, both subspecies migrated to distinct non-breeding ranges within the eastern tropical Pacific Ocean. Observational data identified the general pattern of migration and foraging areas of the species, whereas data from geolocators provided details of routes and timing of migration, core foraging ranges, and marked spatial and temporal segregation between the two subspecies. However, by attaching geolocators only to established breeders, as is typical of studies of small and medium-sized seabirds, these devices failed to identify that non-breeding birds (pre-breeders and adults that are deferring breeding) may not follow the same migratory schedules or have the same at-sea distribution. We conclude that integrating data from electronic tracking with observational data substantially improves our understanding of the pelagic distribution of seabird populations.

Jefferson, TA, Weir CR, Anderson RC, Ballance LT, Kenney RD, Kiszka JJ.  2014.  Global distribution of Risso's dolphin Grampus griseus: a review and critical evaluation. Mammal Review. 44:56-68.   10.1111/mam.12008   AbstractWebsite

The global range of Risso's dolphin Grampus griseus is not well known, and there has been confusion in the literature as to whether the species has a broad, circumglobal range or only occurs along continental margins. To clarify the species' distribution and habitat preferences, we compiled and reviewed all available (published and unpublished) records of sightings and captures of this species for the past 62 years (1950-2012, n=8068 records). Stranding records were not included. The results showed that the species has a range that extends across ocean basins and spans between at least 64 degrees N and 46 degrees S, and is apparently absent from high-latitude polar waters. Although Risso's dolphins occur in all habitats from coastal to oceanic, they show a strong range-wide preference for mid-temperate waters of the continental shelf and slope between 30 degrees and 45 degrees latitude. Although a number of misconceptions about the distributional ecology of Risso's dolphin have existed, this analysis showed that it is a widespread species. It strongly favours temperate waters and prefers continental shelf and slope waters to oceanic depths. These habitat preferences appear to hold throughout much or all of the species' range.

Pitman, RL, Totterdell JA, Fearnbach H, Ballance LT, Durban JW, Kemps H.  2014.  Whale killers: Prevalence and ecological implications of killer whale predation on humpback whale calves off Western Australia. Marine Mammal Science.   10.1111/mms.12182  
2013
Ruiz-Cooley, RI, Ballance LT, McCarthy MD.  2013.  Range Expansion of the Jumbo Squid in the NE Pacific: delta N-15 Decrypts Multiple Origins, Migration and Habitat Use. Plos One. 8   10.1371/journal.pone.0059651   AbstractWebsite

Coincident with climate shifts and anthropogenic perturbations, the highly voracious jumbo squid Dosidicus gigas reached unprecedented northern latitudes along the NE Pacific margin post 1997-98. The physical or biological drivers of this expansion, as well as its ecological consequences remain unknown. Here, novel analysis from both bulk tissues and individual amino acids (Phenylalanine; Phe and Glutamic acid; Glu) in both gladii and muscle of D. gigas captured in the Northern California Current System (NCCS) documents for the first time multiple geographic origins and migration. Phe delta N-15 values, a proxy for habitat baseline delta N-15 values, confirm at least three different geographic origins that were initially detected by highly variable bulk delta N-15 values in gladii for squid at small sizes (< 30 cm gladii length). In contrast, bulk delta N-15 values from gladii of large squid (> 60 cm) converged, indicating feeding in a common ecosystem. The strong latitudinal gradient in Phe delta N-15 values from composite muscle samples further confirmed residency at a point in time for large squid in the NCCS. These results contrast with previous ideas, and indicate that small squid are highly migratory, move into the NCCS from two or more distinct geographic origins, and use this ecosystem mainly for feeding. These results represent the first direct information on the origins, immigration and habitat use of this key "invasive'' predator in the NCCS, with wide implications for understanding both the mechanisms of periodic D. gigas population range expansions, and effects on ecosystem trophic structure.

Fiedler, PC, Redfern JV, Van Noord J, Hall C, Pitman RL, Ballance LT.  2013.  Effects of a tropical cyclone on a pelagic ecosystem from the physical environment to top predators. Marine Ecology Progress Series. 484:1-16.   10.3354/meps10378   AbstractWebsite

Tropical cyclones are environmental disturbances that may have important effects on open-ocean ecosystem structure and function, but their overall impact has rarely been assessed. The Stenella Abundance Research Line Transect and Ecosystem (STARLITE) survey, in August-November 2007, investigated spatial and temporal ecosystem variability in the eastern tropical Pacific Ocean off southwestern Mexico. Oceanographic, plankton, flyingfish, seabird, and cetacean sampling was conducted along eight 170 km transect lines, each of which were surveyed on 2 consecutive days at similar to 3 wk intervals. Tropical storm Kiko passed though the study area on 15-17 October and forced changes in the physical environment and in the ecosystem, from plankton to top predators. Kiko mixed water from beneath the strong, shallow thermocline to the surface. As a result, surface temperature decreased by 0.6 degrees C, the thermocline and chlorophyll maximum layer shoaled by 10-20 m, stratification decreased by 27%, and chlorophyll increased by 33% at the surface and 35% over the euphotic zone. These changes persisted for at least 4 wk. Zooplankton biomass increased by 59% about 3 wk after the phyto plankton increase. Changes in the stomach fullness and diet composition of planktivorous flyingfish were consistent with the increase in zooplankton biomass. Among top predators, the sighting rate of dolphins declined, while the response of seabirds varied by species and was confounded by seasonal migration patterns. Tropical cyclones are a recurrent disturbance in this region. They initiate a bottom-up forcing of the ecosystem, creating persistent patches of higher primary and secondary production, and may be regarded as a disturbance regime.

Guy, TJ, Jennings SL, Suryan RM, Melvin EF, Bellman MA, Ballance LT, Blackie BA, Croll DA, Deguchi T, Geernaert TO, Henry RW, Hester M, Hyrenbach KD, Jahncke J, Kappes MA, Ozaki K, Roletto J, Sato F, Sydeman WJ, Zamon JE.  2013.  Overlap of North Pacific albatrosses with the US west coast groundfish and shrimp fisheries. Fisheries Research. 147:222-234. AbstractWebsite

We used a combination of seabird data (both fishery-dependent and fishery-independent) and fishing-effort data to evaluate the relative fisheries risk of five west coast groundfish fisheries and one shrimp fishery to black-footed (Phoebastria nigripes), short-tailed (P. albatrus) and Laysan albatrosses (P. immutabilis). To assess risk, an overlap index was derived as the product of total fishing effort and at-sea survey density of black-footed albatross. This index was used as the primary tool to estimate overlap with the endangered, relatively rare short-tailed albatross, which show similar habitat utilization from satellite telemetry tracks. Telemetry data indicate Laysan albatross primarily occur offshore beyond observed fishing effort. Black-footed and short-tailed albatross-fishery overlap was highest at the shelf-break (201-1000 m) north of 36 degrees N. Overlap and reported albatross mortality indicate that the sablefish (Anoplopoma fimbria) longline and Pacific hake (Merluccius productus) catcher-processor fisheries pose the greatest risk to these species; the near-shore rockfish (Seabastes spp.) longline, pink shrimp (Pandalus jordani) trawl, California halibut (Paralichthys californicus) trawl, and non-hake groundfish trawl fisheries pose relatively little risk. Implementing proven seabird bycatch-reduction measures will likely minimize albatross mortality in the highest-risk fishery, sablefish longline. (C) 2013 Elsevier B.V. All rights reserved.

Staaf, DJ, Redfern JV, Gilly WF, Watson W, Ballance LT.  2013.  Distribution of ommastrephid paralarvae in the eastern tropical Pacific. Fishery Bulletin. 111:78-89.
2012
Forney, KA, Ferguson MC, Becker EA, Fiedler PC, Redfern JV, Barlow J, Vilchis LI, Ballance LT.  2012.  Habitat-based spatial models of cetacean density in the eastern Pacific Ocean.. Endangered Species Research. 16:113-133.   doi:10.3354/esr00393   AbstractWebsite

Many users of the marine environment (e.g. military, seismic researchers, fisheries) conduct activities that can potentially harm cetaceans. In the USA, Environmental Assessments or Environmental Impact Statements evaluating potential impacts are required, and these must include information on the expected number of cetaceans in specific areas where activities will occur. Typically, however, such information is only available for broad geographic regions, e.g. the entire West Coast of the United States. We present species−habitat models that estimate finer scale cetacean densities within the eastern Pacific Ocean. The models were developed and validated for 22 species or species groups, based on 15 large-scale shipboard cetacean and ecosystem assessment surveys conducted in the temperate and tropical eastern Pacific during the period from 1986 to 2006. Model development included consideration of different modeling frameworks, spatial and temporal resolutions of input variables, and spatial interpolation techniques. For the final models, expected group encounter rate and group size were modeled separately, using generalized additive models, as functions of environmental predictors, including bathymetry, distance to shore or isobaths, sea surface temperature (SST), variance in SST, salinity, chlorophyll, and mixed-layer depth. Model selection was performed using cross-validation on novel data. Smoothed maps of species density (and variance therein) were created from the final models for the California Current Ecosystem and eastern tropical Pacific Ocean. Model results were integrated into a web-interface that allows end-users to estimate densities for specified areas and provides fine-scale information for marine mammal assessments, monitoring, and mitigation.

Pitman, RL, Ballance LT, Bost CA.  2012.  Incidence of wing deformities (‘Angel Wing’) among Masked Boobies at Clipperton Island: life history consequences and insight into etiology.. The Wilson Journal of Ornithology. 124(3):597-602.
2011
Nur, N, Jahncke J, Herzog MP, Howar J, Hyrenbach KD, Zamon JE, Ainley DG, Wiens JA, Morgan K, Ballance LT, Stralberg D.  2011.  Where the wild things are: predicting hotspots of seabird aggregations in the California Current System. Ecological Applications. 21:2241-2257. AbstractWebsite

Marine Protected Areas (MPAs) provide an important tool for conservation of marine ecosystems. To be most effective, these areas should be strategically located in a manner that supports ecosystem function. To inform marine spatial planning and support strategic establishment of MPAs within the California Current System, we identified areas predicted to support multispecies aggregations of seabirds ("hotspots''). We developed habitat-association models for 16 species using information from at-sea observations collected over an 11-year period (1997-2008), bathymetric data, and remotely sensed oceanographic data for an area from north of Vancouver Island, Canada, to the USA/Mexico border and seaward 600 km from the coast. This approach enabled us to predict distribution and abundance of seabirds even in areas of few or no surveys. We developed single-species predictive models using a machine-learning algorithm: bagged decision trees. Single-species predictions were then combined to identify potential hotspots of seabird aggregation, using three criteria: (1) overall abundance among species, (2) importance of specific areas ("core areas'') to individual species, and (3) predicted persistence of hotspots across years. Model predictions were applied to the entire California Current for four seasons (represented by February, May, July, and October) in each of 11 years. Overall, bathymetric variables were often important predictive variables, whereas oceanographic variables derived from remotely sensed data were generally less important. Predicted hotspots often aligned with currently protected areas (e.g., National Marine Sanctuaries), but we also identified potential hotspots in Northern California/Southern Oregon (from Cape Mendocino to Heceta Bank), Southern California (adjacent to the Channel Islands), and adjacent to Vancouver Island, British Columbia, that are not currently included in protected areas. Prioritization and identification of multispecies hotspots will depend on which group of species is of highest management priority. Modeling hotspots at a broad spatial scale can contribute to MPA site selection, particularly if complemented by fine-scale information for focal areas.

2010
Ballance, LT, Whitty T.  2010.  Ecosystem-Based Management for the Oceans. Restoration Ecology. 18:780-781.Website
Olson, RJ, Popp BN, Graham BS, Lopez-Ibarra GA, Galvan-Magana R, Lennert-Cody CE, Bocanegra-Castillo N, Wallagrove NJ, Gier E, Alatorre-Ramirez B, Ballance LT, Fry B.  2010.  Food web inferences of stable isotope spatial patterns in copepods and yellowfin tuna in the pelagic eastern Pacific Ocean.. Progress in Oceanography. 86:124-138.