Publications by authors named "Dennis M Higgs"

17 Publications

  • Page 1 of 1

Collective Behavior in Wild Zebrafish.

Zebrafish 2020 08 9;17(4):243-252. Epub 2020 Jun 9.

School of Life Sciences, Arizona State University, Tempe, Arizona, USA.

Anthropogenic change is expected to alter environments at alarming rates. To predict the impact of modified environments on social behavior, we must study the relationship between environmental features and collective behavior in a genetically tractable model, zebrafish (). Here, we conducted a field study to examine the relationship between salient environmental features and collective behavior in four populations of zebrafish. We found zebrafish in flowing water formed volatile groups, whereas those in still water had more consistent membership and leadership. Groups in fast-flowing water were large (up to 2000 fish) and tightly knit with short nearest neighbor distances, whereas group sizes were smaller (11 fish/group) with more space between individual fish in still and slow-flowing water. These observations point to a possible profound role of water flow in influencing collective behavior in wild zebrafish.
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http://dx.doi.org/10.1089/zeb.2019.1851DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7869874PMC
August 2020

Field assessment of behavioural responses of southern stingrays () to acoustic stimuli.

R Soc Open Sci 2020 Jan 22;7(1):191544. Epub 2020 Jan 22.

Department of Biological Sciences, University of Windsor, 401 Sunset Avenue, Windsor, Ontario Canada, N9B 3P4.

The ability of elasmobranchs to detect and use sound cues has been heavily debated in previous research and has only recently received revived attention. To properly understand the importance of sound to elasmobranchs, assessing their responses to acoustic stimuli in a field setting is vital. Here, we establish a behavioural audiogram of free-swimming male and female southern stingrays () exposed to low-frequency tones. We demonstrate that female stingrays exposed to tones (50-500 Hz) exhibit significant changes in swimming behaviours (increased time spent swimming, decreased rest time, increased surface breaches and increased side swimming with pectoral flapping) at 140 dB re 1 µPa (-2.08 to -2.40 dB re 1 m s) while males exposed to the same tones did not exhibit a change in these behaviours until 160 dB re 1 µPa (-1.13 to -1.21 dB re 1 m s). Our results are the first demonstration of field responses to sound in the Batoidea and show a distinct sensitivity to low-frequency acoustic inputs.
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http://dx.doi.org/10.1098/rsos.191544DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC7029913PMC
January 2020

Neutral genetic variation in adult Chinook salmon () affects brain-to-body trade-off and brain laterality.

R Soc Open Sci 2017 Dec 6;4(12):170989. Epub 2017 Dec 6.

Department of Biological Sciences, University of Windsor, Windsor, Ontario, CanadaN9B 3P4.

Low levels of heterozygosity can have detrimental effects on life history and growth characteristics of organisms but more subtle effects such as those on trade-offs of expensive tissues and morphological laterality, especially of the brain, have not been explicitly tested. The objective of the current study was to investigate how estimated differences in heterozygosity may potentially affect brain-to-body trade-offs and to explore how these heterozygosity differences may affect differential brain growth, focusing on directional asymmetry in adult Chinook salmon () using the laterality and absolute laterality indices. Level of inbreeding was estimated as mean microsatellite heterozygosity resulting in four 'inbreeding level groups' (Very High, High, Medium, Low). A higher inbreeding level corresponded with a decreased brain-to-body ratio, thus a decrease in investment in brain tissue, and also showed a decrease in the laterality index for the cerebellum, where the left hemisphere was larger than the right across all groups. These results begin to show the role that differences in heterozygosity may play in differential tissue investment and in morphological laterality, and may be useful in two ways. Firstly, the results may be valuable for restocking programmes that wish to emphasize brain or body growth when crossing adults to generate individuals for release, as we show that genetic variation does affect these trade-offs. Secondly, this study is one of the first examinations to test the hypothesized relationship between genetic variation and laterality, finding that in Chinook salmon there is potential for an effect of inbreeding on lateralized morphology, but not in the expected direction.
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http://dx.doi.org/10.1098/rsos.170989DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC5750007PMC
December 2017

The effects of stimulus parameters on auditory evoked potentials of Carassius auratus.

J Comp Physiol A Neuroethol Sens Neural Behav Physiol 2017 Nov 23;203(11):945-951. Epub 2017 Aug 23.

Department of Biological Sciences, University of Windsor, 401 Sunset Avenue, Windsor, ON, N9B 3P4, Canada.

Whole-brain responses to sound are easily measured through auditory evoked potentials (AEP), but it is unclear how differences in experimental parameters affect these responses. The effect of varying parameters is especially unclear in fish studies, the majority of which use simple sound types and then extrapolate to natural conditions. The current study investigated AEPs in goldfish (Carassius auratus) using sounds of different durations (5, 10, and 20 ms) and frequencies (200, 500, 600 and 700 Hz) to test stimulus effects on latency and thresholds. We quantified differences in latency and threshold in comparison to a 10-ms test tone, a duration often used in AEP fish studies. Both response latency and threshold were significantly affected by stimulus duration, with latency patterning suggesting that AEP fires coincident with a decrease in stimulus strength. Response latency was also significantly affected by presentation frequency. These results show that stimulus type has important effects on AEP measures of hearing and call for clearer standards across different measures of AEP. Duration effects also suggest that AEP measures represent summed responses of duration-detecting neural circuit, but more effort is needed to understand the neural drivers of this commonly used technique.
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http://dx.doi.org/10.1007/s00359-017-1207-3DOI Listing
November 2017

The Potential Overlapping Roles of the Ear and Lateral Line in Driving "Acoustic" Responses.

Adv Exp Med Biol 2016 ;877:255-70

Leigh Marine Laboratory, Institute of Marine Science, University of Auckland, Auckland, New Zealand.

Examination of fish responses to sound stimuli has a rich and varied history but it is not always clear when responses are true measures of hearing or the lateral-line. The central innervation of auditory and lateral-line sensory afferents lie in close proximity in the brainstem and both sets of receptors are, at heart, hair cell-based particle motion detectors. While it is possible to separately measure physiological activity of these two receptor subtypes, many studies of fish "hearing" use whole brain potentials or behavioural assays in complex sound fields where it is not possible to distinguish inputs. We argue here that, as often measured, what is thought of as fish "hearing" is often a multisensory response of both auditory and lateral line receptors. We also argue that in many situations where fish use sound stimuli, the behaviour is also an integrative response of both systems, due to the often close proximity of fish during sound communication. We end with a set of recommendations for better understanding the separate and combined roles of ear and lateral-line hair cells as well as an acknowledgment of the seminal and continuing contributions of Arthur N. Popper and Richard R. Fay to this field.
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http://dx.doi.org/10.1007/978-3-319-21059-9_12DOI Listing
April 2016

Hearing in Cavefishes.

Adv Exp Med Biol 2016 ;877:187-95

Biological Sciences, University of Windsor, Windsor, ON, Canada, N9B 3P4.

Caves and associated subterranean habitats represent some of the harshest environments on Earth, yet many organisms, including fishes, have colonized and thrive in these habitats despite the complete absence of light, and other abiotic and biotic constraints. Over 170 species of fishes are considered obligate subterranean inhabitants (stygobionts) that exhibit some degree of troglomorphy, including degeneration of eyes and reduction in pigmentation. To compensate for lack of vision, many species have evolved constructive changes to non-visual sensory modalities. In this chapter we review hearing in cavefishes, with particular emphasize on our own studies on amblyopsid cavefishes. Hearing in cavefishes has not been well studied to date, as hearing ability has only been examined in four species. Two species show no differences in hearing ability relative to their surface relatives, while the other two species (family Amblyopsidae) exhibit regression in the form of reduced hearing range and reduction in hair cell densities on sensory epithelia. In addition to reviewing our current knowledge on cavefish hearing, we offer suggestions for future avenues of research on cavefish hearing and discuss the influence of Popper and Fay on the field of cavefish bioacoustics.
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http://dx.doi.org/10.1007/978-3-319-21059-9_9DOI Listing
April 2016

Sublethal effects of cadmium on auditory structure and function in fathead minnows (Pimephales promelas).

Fish Physiol Biochem 2015 Apr 23;41(2):357-69. Epub 2014 Sep 23.

Department of Biological Sciences, University of Windsor, 401 Sunset Avenue, Windsor, ON, N9B 3P4, Canada.

Aquatic ecosystems are threatened by environmental contaminants, and many heavy metals can influence both the structure and function of sense organs in fishes. The use of these senses is vital to the survival and reproductive success of fish and therefore affects the health of the ecosystem as a whole. The current study examines the effects of cadmium on auditory structure and function in the fathead minnow (Pimephales promelas). In the laboratory, fish were exposed for 96 h to a range of cadmium concentrations and both hearing sensitivity and hair cell morphology were quantified. While hair cell numbers were unaffected, cadmium caused an increase in auditory threshold, with a critical range for toxic effects of cadmium estimated at 2.1-2.9 µg L(-1). Cadmium exposure also caused a decrease in response latency at higher cadmium concentrations. The current study demonstrates the sublethal effects of cadmium on fish sensory function while also pointing to the need for more careful interpretation of cadmium impacts on aquatic populations.
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http://dx.doi.org/10.1007/s10695-014-9988-6DOI Listing
April 2015

Multigenerational outbreeding effects in Chinook salmon (Oncorhynchus tshawytscha).

Genetica 2014 Aug 22;142(4):281-93. Epub 2014 Jun 22.

Great Lakes Institute for Environmental Research, University of Windsor, Ontario, N9B 3P4, Canada,

Outbreeding, mating between genetically divergent individuals, may result in negative fitness consequences for offspring via outbreeding depression. Outbreeding effects are of notable concern in salmonid research as outbreeding can have major implications for salmon aquaculture and conservation management. We therefore quantified outbreeding effects in two generations (F1 hybrids and F2 backcrossed hybrids) of Chinook salmon (Oncorhynchus tshawytscha) derived from captively-reared purebred lines that had been selectively bred for differential performance based on disease resistance and growth rate. Parental lines were crossed in 2009 to create purebred and reciprocal hybrid crosses (n = 53 families), and in 2010 parental and hybrid crosses were crossed to create purebred and backcrossed hybrid crosses (n = 66 families). Although we found significant genetic divergence between the parental lines (FST = 0.130), reciprocal F1 hybrids showed no evidence of outbreeding depression (hybrid breakdown) or favorable heterosis for weight, length, condition or survival. The F2 backcrossed hybrids showed no outbreeding depression for a suite of fitness related traits measured from egg to sexually mature adult life stages. Our study contributes to the current knowledge of outbreeding effects in salmonids and supports the need for more research to better comprehend the mechanisms driving outbreeding depression.
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http://dx.doi.org/10.1007/s10709-014-9774-5DOI Listing
August 2014

Evidence for hearing loss in amblyopsid cavefishes.

Biol Lett 2013 Jun 27;9(3):20130104. Epub 2013 Mar 27.

Department of Ecology and Evolutionary Biology, Yale University, New Haven, CT 06520, USA.

The constant darkness of caves and other subterranean habitats imposes sensory constraints that offer a unique opportunity to examine evolution of sensory modalities. Hearing in cavefishes has not been well explored, and here we show that cavefishes in the family Amblyopsidae are not only blind but have also lost a significant portion of their hearing range. Our results showed that cave and surface amblyopsids shared the same audiogram profile at low frequencies but only surface amblyopsids were able to hear frequencies higher than 800 Hz and up to 2 kHz. We measured ambient noise in aquatic cave and surface habitats and found high intensity peaks near 1 kHz for streams underground, suggesting no adaptive advantage in hearing in those frequencies. In addition, cave amblyopsids had lower hair cell densities compared with their surface relative. These traits may have evolved in response to the loud high-frequency background noise found in subterranean pools and streams. This study represents the first report of auditory regression in a subterranean organism.
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http://dx.doi.org/10.1098/rsbl.2013.0104DOI Listing
http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3645044PMC
June 2013

Condition-dependent auditory processing in the round goby (Neogobius melanostomus): links to sex, reproductive condition and female estrogen levels.

J Exp Biol 2013 Mar 29;216(Pt 6):1075-84. Epub 2012 Nov 29.

Department of Biological Sciences, University of Windsor, Windsor, ON, Canada, N9B 3P4.

Neural responses to sensory stimuli often differ between sexes, vary seasonally, and can be regulated by endocrine activity, but the ecological and physiological mechanisms driving such patterns are not well understood. The current study examined how auditory function in the round goby (Neogobius melanostomus), a vocal teleost, co-varied with sex, reproductive condition and female plasma 17β-estradiol level. Auditory evoked potentials were collected in response to tone pips (100-600 Hz) and a natural round goby pulse vocalization. Additionally, saccule hair cell densities were compared across reproductive groups. Auditory threshold was evaluated in terms of pressure and particle acceleration, and response amplitude and onset latency were measured at 10 dB above threshold. Relative to males, females displayed lower auditory thresholds in response to the natural vocalization and to tones at 300-600 Hz, and had a higher density of saccule hair cells. The 17β-estradiol level was positively associated with amplitude and latency for the pulse stimulus and with both threshold and amplitude for tones at 100-200 Hz in females. Relative to non-reproductive males, reproductive males exhibited longer response latencies at 100-200 Hz. The results demonstrate sexual dimorphism in auditory function in a teleost fish as well as intra-sexual variation, partially based on hormone levels. The current research further identifies links between auditory function and reproductive behaviors in fishes and provides a finer-scaled analysis of how this behavior is reflected at the level of the sensory systems facilitating signal reception.
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http://dx.doi.org/10.1242/jeb.076935DOI Listing
March 2013

Pressure and particle motion detection thresholds in fish: a re-examination of salient auditory cues in teleosts.

J Exp Biol 2012 Oct 12;215(Pt 19):3429-35. Epub 2012 Jun 12.

Leigh Marine Laboratory, University of Auckland, Warkworth 0941, New Zealand.

The auditory evoked potential technique has been used for the past 30 years to evaluate the hearing ability of fish. The resulting audiograms are typically presented in terms of sound pressure (dB re. 1 μPa) with the particle motion (dB re. 1 m s(-2)) component largely ignored until recently. When audiograms have been presented in terms of particle acceleration, one of two approaches has been used for stimulus characterisation: measuring the pressure gradient between two hydrophones or using accelerometers. With rare exceptions these values are presented from experiments using a speaker as the stimulus, thus making it impossible to truly separate the contribution of direct particle motion and pressure detection in the response. Here, we compared the particle acceleration and pressure auditory thresholds of three species of fish with differing hearing specialisations, goldfish (Carassius auratus, weberian ossicles), bigeye (Pempheris adspersus, ligamentous hearing specialisation) and a third species with no swim bladder, the common triplefin (Forstergyian lappillum), using three different methods of determining particle acceleration. In terms of particle acceleration, all three fish species have similar hearing thresholds, but when expressed as pressure thresholds goldfish are the most sensitive, followed by bigeye, with triplefin the least sensitive. It is suggested here that all fish have a similar ability to detect the particle motion component of the sound field and it is their ability to transduce the pressure component of the sound field to the inner ear via ancillary hearing structures that provides the differences in hearing ability. Therefore, care is needed in stimuli presentation and measurement when determining hearing ability of fish and when interpreting comparative hearing abilities between species.
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http://dx.doi.org/10.1242/jeb.073320DOI Listing
October 2012

Behavioral measure of frequency detection and discrimination in the zebrafish, Danio rerio.

Zebrafish 2012 Mar 22;9(1):1-7. Epub 2012 Feb 22.

Department of Biological Sciences, University of Windsor, Windsor, Ontario, Canada.

Behavioral tests of hearing in fish are relatively rare and are generally based upon aversive conditioning, with little data available for the positive reinforcement methods common in other vertebrates. Despite its increasing importance as an auditory model, no behavioral hearing measures have been conducted on zebrafish (Danio rerio), with only physiological hearing estimates available. In the current study, a new behavioral testing paradigm is developed to assess sound detection abilities of zebrafish and the effect of training frequency on hearing sensitivity. Zebrafish were trained to respond to either a 400 Hz or a 1000 Hz tone, and behavioral thresholds were then measured to tones from 200 to 1000 Hz. Significant threshold differences existed between the behavioral audiograms, with fish from each set most sensitive to their conditioned frequency. Furthermore, fish acoustically conditioned to 1000 Hz were most sensitive to the upper range of test frequencies (600-1000 Hz). This appears to be the first study utilizing a positive reinforcement behavioral assay for testing hearing in zebrafish and provides further evidence of fine-scale auditory filtering in fish.
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http://dx.doi.org/10.1089/zeb.2011.0720DOI Listing
March 2012

Assessing disturbance from under-ice noise on fishes in boreal lakes.

Adv Exp Med Biol 2012 ;730:363-6

Department of Fisheries and Oceans, Yellowknife, Canada.

There are many potential sources of anthropogenic noise that can manifest under ice in boreal lakes that are within the hearing ranges of northern boreal fishes. Impacts of noise on fish can be correlated to the fish's hearing sensitivity. In general, boreal fishes have most sensitive hearing <400 Hz,but this varies by species and life stage. By assessing the hearing capabilities and vocalizations of fish species and sound signatures from development activities, it may be possible to forecast potential impacts resulting from expected under-ice noise exposure.There is still the need for basic information to facilitate the assessment and identification of potential impacts (e.g., the hearing capabilities of many species of boreal fishes at different life stages and the sound signatures of various anthropogenic noise sources). Additionally, the impacts to fish from a particular noise source (e.g., pile driving) or the potential for a sound-related disturbance ata particular time in a species life history, such as courtship or spawning, warrants further study.
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http://dx.doi.org/10.1007/978-1-4419-7311-5_82DOI Listing
April 2012

Dispersal strategies, secondary range expansion and invasion genetics of the nonindigenous round goby, Neogobius melanostomus, in Great Lakes tributaries.

Mol Ecol 2011 May 24;20(9):1845-59. Epub 2011 Feb 24.

Great Lakes Institute for Environmental Research, University of Windsor, 401 Sunset Ave. Windsor, ON N9B 3P4, Canada.

Dispersal strategies are important mechanisms underlying the spatial distribution and colonizing ability of all mobile species. In the current study, we use highly polymorphic microsatellite markers to evaluate local dispersal and colonization dynamics of the round goby (Neogobius melanostomus), an aquatic invader expanding its range from lake to river environments in its introduced North American range. Genetic structure, genotype assignment and genetic diversity were compared among 1262 round gobies from 20 river and four lake sites in three Great Lakes tributaries. Our results indicate that a combination of short-distance diffusion and long-distance dispersal, collectively referred to as 'stratified dispersal', is facilitating river colonization. Colonization proceeded upstream yearly (approximately 500 m/year; 2005-2009) in one of two temporal replicates while genetic structure was temporally stable. Contiguous dispersal from the lake was observed in all three rivers with a substantial portion of river fish (7.3%) identified as migrants. Genotype assignment indicated a separate introduction occurred upstream of the invasion front in one river. Genetic diversity was similar and relatively high among lake and recently colonized river populations, indicating that founder effects are mitigated through a dual-dispersal strategy. The remarkable success of round goby as an aquatic invader stresses the need for better diffusion models of secondary range expansion for presumably sessile invasive species.
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http://dx.doi.org/10.1111/j.1365-294X.2011.05030.xDOI Listing
May 2011

Audition in sciaenid fishes with different swim bladder-inner ear configurations.

J Acoust Soc Am 2006 Jan;119(1):439-43

Department of Biology & Neuroscience and Cognitive Science Program, University of Maryland, College Park, Maryland 20742, USA.

We investigated how morphological differences in the auditory periphery of teleost fishes may relate to hearing capabilities. Two species of western Atlantic sciaenids were examined: weakfish (Cynoscion regalis, Block and Schneider) and spot (Leiostomus xanthurus, Lacepede). These species differ in the anatomical relationship between the swim bladder and the inner ear. In weakfish, the swim bladder has a pair of anterior horns that terminate close to the ear, while there are no extensions of the swim bladder in spot. Thus, the swim bladder in spot terminates at a greater distance from the ear when compared to weakfish. With the use of the auditory brainstem response technique, Cynoscion regalis were found to detect frequencies up to 2000 Hz, while Leiostomus xanthurus detected up to 700 Hz. There were, however, no significant interspecific differences in auditory sensitivity for stimuli between 200 and 700 Hz. These data support the hypothesis that the swim bladder can potentially expand the frequency range of detection.
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http://dx.doi.org/10.1121/1.2139068DOI Listing
January 2006

Development of form and function in peripheral auditory structures of the zebrafish (Danio rerio).

J Acoust Soc Am 2003 Feb;113(2):1145-54

Department of Biology, University of Maryland, College Park, Maryland 20742, USA.

Investigations of the development of auditory form and function have, with a few exceptions, thus far been largely restricted to birds and mammals, making it difficult to postulate evolutionary hypotheses. Teleost fishes represent useful models for developmental investigations of the auditory system due to their often extensive period of posthatching development and the diversity of auditory specializations in this group. Using the auditory brainstem response and morphological techniques we investigated the development of auditory form and function in zebrafish (Danio rerio) ranging in size from 10 to 45 mm total length. We found no difference in auditory sensitivity, response latency, or response amplitude with development, but we did find an expansion of maximum detectable frequency from 200 Hz at 10 mm to 4000 Hz at 45 mm TL. The expansion of frequency range coincided with the development of Weberian ossicles in zebrafish, suggesting that changes in hearing ability in this species are driven more by development of auxiliary specializations than by the ear itself. We propose a model for the development of zebrafish hearing wherein the Weberian ossicles gradually increase the range of frequencies available to the inner ear, much as middle ear development increases frequency range in mammals.
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http://dx.doi.org/10.1121/1.1536185DOI Listing
February 2003

Age- and size-related changes in the inner ear and hearing ability of the adult zebrafish (Danio rerio).

J Assoc Res Otolaryngol 2002 Jun;3(2):174-84

Department of Biology, University of Maryland, College Park 20742, USA.

Fishes, unlike most other vertebrate groups, continue to add sensory hair cells to their ears for much of their lives. However, it is not clear whether the addition ever stops or how the addition of sensory cells impacts hearing ability. In this article, we tested both questions using the zebrafish, Danio rerio. Our results not only have important implications for understanding the consequences of adding sensory receptors, but these results for normal zebrafish also serve as valuable baseline information for future studies of select mutations on the ear and hearing of this species. Our results show that hair cell production continues in uncrowded zebrafish up to 10 months of age (about one-third of a normal life span), but despite this addition there is no change in hearing sensitivity or bandwidth. Therefore, hearing is not related to the number of sensory cells in the ear in juvenile and adult animals. We also show that despite no net addition of hair cells after about 10 months, hair cells are still being produced, but at a lower rate, presumably to replace cells that are dying. Moreover, crowding of zebrafish has a marked impact on the growth of the fish and on the addition of sensory cells to the ear. We also demonstrate that fish size, not age, is a better indicator of developmental state of zebrafish.
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http://www.ncbi.nlm.nih.gov/pmc/articles/PMC3202399PMC
http://dx.doi.org/10.1007/s101620020035DOI Listing
June 2002