Using the otolith sulcus to aid in prey identification and improve estimates of prey size in diet studies of a piscivorous predator

Diet studies are fundamental for understanding trophic connections in marine ecosystems. In the southeastern US, the common bottlenose dolphin Tursiops truncatus is the predominant marine mammal in coastal waters, but its role as a top predator has received little attention. Diet studies of piscivorous predators, like bottlenose dolphins, start with assessing prey otoliths recovered from stomachs or feces, but digestive erosion hampers species identification and underestimates fish weight (FW). To compensate, FW is often estimated from the least affected otoliths and scaled to other otoliths, which also introduces bias. The sulcus, an otolith surface feature, has a species‐specific shape of its ostium and caudal extents, which is within the otolith edge for some species. We explored whether the sulcus could improve species identification and estimation of prey size using a case study of four sciaenid species targeted by fisheries and bottlenose dolphins in North Carolina. Methods were assessed first on otoliths from a reference collection (n = 421) and applied to prey otoliths (n = 5,308) recovered from 120 stomachs of dead stranded dolphins. We demonstrated in reference‐collection otoliths that cauda to sulcus length (CL:SL) could discriminate between spotted seatrout (Cynoscion nebulosus) and weakfish (Cynoscion regalis) (classification accuracy = 0.98). This method confirmed for the first time predation of spotted seatrout by bottlenose dolphins in North Carolina. Using predictive models developed from reference‐collection otoliths, we provided evidence that digestion affects otolith length more than sulcus or cauda length, making the latter better predictors. Lastly, we explored scenarios of calculating total consumed biomass across degrees of digestion. A suggested approach was for the least digested otoliths to be scaled to other otoliths iteratively from within the same stomach, month, or season as samples allow. Using the otolith sulcus helped overcome challenges of species identification and fish size estimation, indicating their potential use in other diet studies.     

Validation of daily otolith increments in larval and juvenile Chinese sucker, <Emphasis Type="Italic">Myxocyprinus asiaticus</Emphasis>

Otolith development was observed and the formation of daily growth increments in otoliths of Chinese sucker, Myxocyprinus asiaticus, was validated by monitoring known-age larvae and juveniles in the laboratory from 2003 to 2005. Otolith shape changed with larval and juvenile development, and there was an exponential relationship until a body length of 16 mm or so, and a linear relationship after a body length of 16 mm between otolith size and fish size. The first increment was identified in larvae 1 day after hatching. The regressed equations between daily age (D) and increment number in otoliths (N) were N = −0.64 + 0.96D in lapillus, and N = −0.31 + 0.98D in sagitta. The slopes were not significantly different than 1.0. This demonstrated that otolith increments in this species were formed daily and can be used for daily age determination.     

Otolith formation,microstructure and daily increment validation in juvenile perch Perca fluviatilis

The otoliths of laboratory‐reared larval and juvenile perch Perca fluviatilis of known age were analysed to determine the age of otolith formation and validate the formation of daily increments. There was a linear relationship between number of increments and age in days post‐hatching, although by 82 days post‐hatching daily increment counts underestimated actual age by an average of 5 days. Otolith dimensions in relation to standard length indicated allometric growth of otoliths until completion of yolk absorption, and isometric growth thereafter, up to 82 days post‐hatching.     

Enigmatic ear stones: what we know about the functional role and evolution of fish otoliths

Otoliths in bony fishes play an important role in the senses of balance and hearing. Otolith mass and shape are, among others, likely to be decisive factors influencing otolith motion and thus ear functioning. Yet our knowledge of how exactly these factors influence otolith motion is incomplete. In addition, experimental studies directly investigating the function of otoliths in the inner ear are scarce and yield partly conflicting results. Herein, we discuss questions and hypotheses on how otolith mass and shape, and the relationship between the sensory epithelium and overlying otolith, influence otolith motion. We discuss (i) the state‐of‐the‐art knowledge regarding otolith function, (ii) gaps in knowledge that remain to be filled, and (iii) future approaches that may improve our understanding of the role of otoliths in ear functioning. We further link these functional questions to the evolution of solid teleost otoliths instead of numerous tiny otoconia as found in most other vertebrates. Until now, the selective forces and/or constraints driving the evolution of solid calcareous otoliths and their diversity in shape in teleosts are largely unknown. Based on a data set on the structure of otoliths and otoconia in more than 160 species covering the main vertebrate groups, we present a hypothetical framework for teleost otolith evolution. We suggest that the advent of solid otoliths may have initially been a selectively neutral ‘by‐product’ of other key innovations during teleost evolution. The teleost‐specific genome duplication event may have paved the way for diversification in otolith shape. Otolith shapes may have evolved along with the considerable diversity of, and improvements in, auditory abilities in teleost fishes. However, phenotypic plasticity may also play an important role in the creation of different otolith types, and different portions of the otolith may show different degrees of phenotypic plasticity. Future studies should thus adopt a phylogenetic perspective and apply comparative and methodologically integrative approaches, including fossil otoliths, when investigating otoconia/otolith evolution and their function in the inner ear.     

Relationships between fish size and otolith size of four bathydemersal fish species from the south eastern Arabian Sea,India

The objective of this study was to estimate a prey body size from the hard parts (e.g. otoliths) of a fish species frequently found in the guts of predators. Length–weight relationships between otolith size (length, height, weight and aspect ratio) and fish size (total length and weight) were determined for four fish species captured in the Arabian Sea by bottom trawl (2015 survey on‐board FORV Sagar Sampada, 200–300 m depth), off the west coast of India: Psenopsis cyanea, Pterygotrigla hemisticta, Bembrops caudimacula and Hoplostethus rubellopterus. No significant differences were noted between the size of the left and right otoliths (t test) in any of the four species. The length–weight relationship of the otolith in all four species showed a negative allometric growth pattern (t test, p < .05). The data fitted well to the regression model for otolith length (OL), otolith height (OH) and otolith weight (OW) to total length (TL) and total weight (TW). Results showed that these relationships are a helpful tool in predicting fish size from the otoliths and in calculating the biomass of these less‐studied fish species during feeding studies and palaentology.     

Relationships between fish and otolith size of nine deep‐sea fishes from the Andaman and Nicobar waters,North Indian Ocean

The study presents for the first time the otolith morphology of nine species of deep‐sea fishes. This study was based on sampling carried out on‐board FORV Sagar Sampada (Cruise No 349) during March‐April 2016, along the continental margin of the Andaman and Nicobar Islands in the Bay of Bengal using high speed demersal trawl. Unbroken (complete) otoliths from Polymixia fusca Kotthaus, 1970, Neoepinnula orientalis (Gilchrist & von Bonde 1924), Chlorophthalmus nigromarginatus (Kamohara, 1953), Cubiceps baxteri (McCulloch, 1923), Bembrops caudimacula (Steindachner, 1876), Neoscopelus microchir (Matsubara, 1943), Ostracoberyx dorygenis Fowler, 1934, Synagrops japonicus (Döderlein, 1883), and Bathyclupea hoskynii Alcock 1891) were used for this study. Length–weight relationships (LWR) and the regression between otolith size (width, weight, area and perimeter) and fish length (TL) of nine deep‐sea Fishes were considered. Numerical relationships derived from the relationship between otolith size and the fish can be used as predictors to estimate the prey size as well as to understand trophic relations and food web dynamics of these hitherto unexamined deep‐sea ichthyofauna. LWR showed negative allometric otolith growth in five species; four species showed positive allometric growth. Otolith size to fish size (TL) relation is explained by a simple linear regression considering otolith width (OW), otolith weight (OWe), otolith area (OA) and otolith perimeter (OP). Stronger r² values (>.76) indicate robustness, except for Cubiceps baxteri (r² = .65), and give better estimates for the TL of the fish.     

Discrimination of red porgy Pagrus pagrus (Sparidae) potential stocks in the south-western Atlantic by otolith shape analysis

Otolith shape analysis is a powerful method for fish stock identification. We compared the otolith shape of Pagrus pagrus (Linnaeus 1758) along with its distribution in four south-western Atlantic regions where it is commercially fished: Rio de Janeiro, Rio Grande do Sul in southern Brazil, the Argentine-Uruguayan Common Fishing Zone (UA) and the Argentinian Exclusive Fishing Zone (AR). Otolith shapes were compared by Elliptical Fourier and Wavelet coefficients among specimens in a size range with similar otoliths, morphometric parameters and ages. Four potential stocks were identified: one in the AR, a second along the UA which included specimens from southern Brazil with well-marked opaque bands in its otoliths (MRS), the third in southern Brazil with faint or absent opaque bands in its otoliths (FRS) and the fourth along Rio de Janeiro. The difference in the otolith shape among regions followed differences reported using other stock identification techniques. The similarity between otoliths from UA and MRS (ANOVA-like, P > 0.01) can be explained by seasonal short-range migrations. Otoliths shape differences between MRS and FRS (ANOVA-like, P < 0.01) suggest that P. pagrus does not form a homogeneous group in southern Brazil.     

Assessment of errors associated with harbour seal (Phoca vitulina) faecal sampling

Six harbour seals, ages 4–8 years, were held as pairs in a 10 times 20 times 2 m tank filled with sea water, and on 60 occasions were fed a meal of a specific species of fish or cephalopod of known size. The tank was drained periodically, and harbour seal faeces were collected on a 0.5 mm sieve. Number and size of otoliths and beaks found in faeces were determined. Fifty-eight percent of 670 fish and 37% of 36 cephalopods fed to harbour seals were represented by their otoliths or beaks in faeces. Estimated number of prey consumed was determined from the greatest number of left or right otoliths or upper or lower beaks collected in faeces. Estimated length ofprey was determined from measurements of otoliths and beaks recovered in the tank and relationships of otolith and beak measurements to prey length. Estimated number of fish eaten was not significantly different among pairs of harbour seals, but was different among species of fishes. Only 24–35% of fish species with small otoliths were represented in faeces, whereas more robust otoliths from other species were less apt to be completely dissolved. Estimated length of fishes was significantly less than lengths of fishes fed to harbour seals in 39 (76.5%) of 51 trials. Cephalopod beaks were not affected by passage through the harbour seal digestive tract. Amount of otolith dissolution was not related to species of fish; estimated fish length was underestimated by an average 27.5%. Although some (7.4%) of the otoliths were collected within 100 h after the fish were ingested, more than 90% were recovered within 24 h after the fish was eaten. Correction factors were developed which will allow researchers to estimate more reliably number and size of fish and cephalopod prey eaten by harbour seals.     

Growth and otolith microstructure of cod (Gadus morhua L.) larvae

Cod larvae from Irish Sea stocks were reared under differentgrowth conditions, and the otolith growth and increment formationexamined in sagittae and lapilli. Otolith increments were firstdeposited around the time of hatching and increment counts,on average, reflected larval age. The growth rate of fish larvaereared in different sized tanks was significantly different(P < 0.001), but there was no detectable effect on incrementformation. Otolith size was independent of larval size for individuals<5 mm in length. In larvae >6 mm, larger, faster growingindividuals had larger and faster growing otoliths.     

Morphology and taxonomic significance of the otoliths of some bathypelagic Anguilloidei and Saccopharyngoidei from the Sargasso Sea

The sagittal otoliths of seven anguilliform species belonging to the families Nemichthyidae, Serrivomeridae and Eurypharyngidae are described and illustrated, and a key for their identification is provided. Although the leptocephali of the various fish species treated here have similar otoliths, some species develop specific otolith characteristics during the adult stage. The shape as well as the ratio of fish length to otolith length ratio in adults may serve as a taxonomic aid. Since the sagittae of these fishes can be used for specific identification, the digested remains of prey in the stomachs and guts of predators can be identified.     

Fish otoliths: do sizes correlate with taxonomic group,habitat and/or luminescence?

Otoliths are dense structures in the ears of fishes that function in hearing and gravity perception. Otolith (sagitta) diameters, as percentages of standard length (% SL), are calculated for 247 marine fish species in 147 families and compared by taxonomic group (usually order), habitat and presence or absence of luminescence. Otolith sizes range from 0.4-31.4 mm and 0.08-11.2% SL. The eel and spiny eel orders Anguilliformes and Notacanthiformes have small to very small otoliths, as do the triggerfish order Tetraodontiformes, pipefish order Gasterosteiformes, billfish suborder Scombroidei and many of the dragonfish order Stomiiformes. The soldierfish order Beryciformes has moderate to very large otoliths. The perch order Perciformes has a wide range of otolith sizes but most have small to moderate otoliths 2-5% SL. Only 16 out of the 247 species have the relatively largest otoliths, over 7% SL. Seven out of these 16 species are also luminous from a variety of habitats. Luminous species have slightly to much larger otoliths than non-luminous species in the same family Both beryciforms and luminous fishes live in low-light environments, where acute colour vision is probably impossible. Most fishes of the epipelagic surface waters have very small otoliths, perhaps due to background noise and/or excessive movement of heavy otoliths in rough seas. Bathypelagic species usually have small otoliths and regressed or absent swimbladders. Other habitats have species with a range of otolith sizes. While the relationship between hearing ability and otolith length is unknown, at least some groups with modified swim-bladders have larger otoliths, which may be associated with more acute hearing.     

Lesser Sandplover,Charadrius mongolus,in Turkey

Sagittal otoliths are widely used to determine taxon, age and size of the teleost fishes, and are useful tools for studies of prey-predator relationships, population dynamics and ichthyo-archaeology. They can also be used to estimate the size of the prey. We examined the relationships between otolith measurements (length, height and weight) and fish size (total length and weight) for two species of Argentinidae (Argentina sphyraena and Glossanodon leioglossus) from the Southern Aegean Sea, Turkey. Length, height and mass of sagittae were shown to be good indicators for the length and weight of fish in both species. Glossanodon leioglossus has relatively larger sagittae than Argentina sphyraena. Linear and exponential functions provided the best fit for relations between otolith and fish measurements. No significant differences were found between left and right otolith sizes.     

Correlations between body length and otolith size in smallmouth bass Micropterus dolomieu Lacépède, 1802 with implications for retrospective growth analyses

Reconstructing individual growth history from analysis of increments in otoliths, scales, or spines can provide information on past growth responses to environmental variation, which in turn can be useful for predicting population‐level response to climate change. The objective of this study was to examine correlations between body length and different metrics of otolith size for Micropterus dolomieu. Three metrics corresponding to commonly‐used microstructural and ultrastructural otolith dimensions were measured using image analysis of digital micrographs from a sample of 214 M. dolomieu ranging from 115 to 438 mm total length collected in 2011–2013. It was found that anteroposterior length of whole otoliths provided much improved regression relationships with body size as well as ease of data collection and faster sampling throughput compared with microstructural measures from polished sections. When applying these metrics to reconstruct growth history the biological intercept model generally produced more reasonable back‐calculated estimates of length‐at‐age, although this was not consistent across all otolith metrics. Results suggest that whole otolith measures should be employed due to efficiency of data collection and greater reliability for reconstructing growth history in M. dolomieu.     

Rhythmic structural and chemical patterns in otoliths of the Antarctic fish Notothenia larseni: Their application to age determination

Summary Sagittal otoliths from Notothenia larseni contain microincremental growth rings which are distinctly visible in otolith sections using Scanning Electron Microscopy. These microincrements are similar to those deposited daily in the otoliths of fishes from temperate and tropical waters. Microincrements were easily enumerated and fish length was related to increment number by a logarithmic curve. Otolith microstructure analysis appears to provide a technique to accurately determine age and growth rates in these fish. Sr/Ca ratios in otolith aragonite were analyzed along a radius from the outside edge to the core of an otolith section using an electron microprobe. The strontium/calcium (Sr/Ca) ratios varied with a cyclic periodicity apparently related to seasonal water temperature cycles and the number of cycles agreed closely with age estimated from daily microincrement counts. Sr/ca cycles can potentially be used to determine age, validate growth rates determined by other methods, and establish thermal conditions experienced during the life of a fish. Microstructural and chemical analyses of otoliths demonstrate great potential in helping to answer many questions about the growth processes and ecology of Antarctic fishes.     

Estimates on age,growth and mortality of the French angelfish Pomacanthus paru (Bloch, 1787) (Teleostei: Pomacanthidae) in the southwestern Atlantic

The aim of the present study was to determine age, growth and mortality of the French angelfish Pomacanthus paru. Age was solely determined by sectioned otoliths. All tetracycline‐treated otoliths were 1 year of age and revealed a clear fluorescent mark when observed under UV light. Otolith weight increased exponentially with standard length, and linearly with age, indicating that otolith growth continues with age and is independent of size. Age of fish in the sample ranged from 1 to 27 years. The von Bertalanffy growth equation was TLt = 36.33 (1 ? e^{?0.12 (t + 0)}). Total rate mortality (Z) was estimated to be 0.10. Attaining maximal size slowly, P. paru has a long life expectancy. Most linear growth is achieved within approximately 74% of the lifetime of the fish. Besides being an important ornamental species, P. paru has been commonly captured for decades as bycatch in trap fisheries. These growth parameters should be used with the purpose of managing fisheries targeting this species before more meaningful limits can be imposed. In the aquarium trade management, it is suggested that conservationist issues should be based on capture‐per‐area and the establishment of protected areas.     

The relationship between otolith size and estimated age of tigertooth croaker (Otolithes ruber Bloch and Schneider, 1801) in Oman Sea,Iran

The relationships between somatic growth and otolith dimensions, otolith size to estimated age and growth parameters of the tigertooth croaker (Otolithes ruber) were investigated in 100 specimens (size range: 19.1–52.0 cm, total length) from the Oman Sea area, September 2014. All 100 otoliths were sectioned and determined by age. The oldest specimen was a 4.5‐year‐old female with a total length of 40.6 cm; the youngest specimen was also a female estimated at 1 year of age with a total length of 19.1 cm. The von Bertalanffy growth equation was estimated as L_t = 54.70 (1 ? exp (?0.37 (t + 0.21))). Concluded was that there is a significant relationship between body size, otolith dimensions and estimated age of Otolithes ruber.     

Otolith Microstructure of Larval Gymnocypris potanini Herzenstein from the Minjiang River in China

Synopsis Otolith microstructure of about 120 Gymnocypris potanini larvae from the Minjiang River in China was examined and analyzed. Larvae had multiple primordia in most lapilli and sagittae, while had only one primordium in a few specimens. There had only one nucleus in otoliths of the larvae, except for some few specimens with 2 nuclei. The transparence of many otoliths differed from center to edge, and part of them could be divided into inner low optically dense zone (LODZ) and outer optically dense zone (ODZ). Based on increment clarity, otoliths of this species could be classified into three types, which were otolith with subtile increments, otolith with almost identified increments, and otolith with fairly clear increments characterized by high contrast. The last two types of otolith accounted for 87.07% in lapilli and 94.46% in sagittae, respectively. Increment clarity of sagitta was higher than that of lapillus. Natural checks were identified in 32.50% lapilli and 48.33% sagittae. These checks primarily located in the first to sixth increment. According to the number of increments in otoliths, the age of this batch larvae was 14 – 22 days, birth date was on June 17 – 25, and average growth rate of body length was 0.8936 ± 0.08769 mm/d.     

Age and growth of Alburnus tarichi (Güldenstädt, 1814): an endemic fish species of Lake Van (Turkey)

In total, 240 tarek, Alburnus tarichi, specimens were caught throughout February 2008 in Lake Van, Turkey, a lake with highly salty‐alkaline conditions. Ages, lengths and weights of A. tarichi were determined to estimate length–weight relationships and age composition. Otolith dimensions were also determined. Female : male ratio was 1.47 : 1. Fork length and total weight of specimens ranged from 14.3 to 19.2 cm and 45.76 to 99.63 g, respectively. Maximum age observed was 6 years. Length–weight relationships were calculated for female, male and combined sexes as, W = 0.057FL^2.582W = 0.102FL^2.513 W = 0.074FL^2.544, respectively. Concerning types of growth, negative allometric growth (b < 3) was observed for all tarek specimens. The lagenar otolith was large and flat and marks on otoliths were typically clear, consistent and easy to interpret. Mean otolith length, breadth and weight were determined as 2.592 mm, 2.381 mm, 0.0026 g, respectively. While the otolith weight displayed a curvilinear relationship with the fork length, otolith length and breadth were linearly related to the fork length by height correlation coefficients.     

Prey selection by age-0 walleye pollock, Theragra chalcogramma, in nearshore waters of the Gulf of Alaska

Juvenile walleye pollock, Theragra chalcogramma, is the dominant forage fish on the continental shelf of the Gulf of Alaska, yet little is known about the feeding habits of this important interval of pollock life history. The taxonomic composition and size of prey found in the stomachs of age-0 juveniles collected at three nearshore locations in the Gulf of Alaska in September 1990 were compared to the composition and size of zooplankton collected in concurrent plankton tows. The maximum length of prey consumed increased dramatically over the length range of pollock examined (58–110 mm) from approximately 7 mm to 30 mm, due mainly to the consumption of large euphausiids and chaetognaths by the bigger individuals. The maximum width of prey changed little over this size range although there was a general increase in prey width with increasing predator size. The minimum prey length and width did not change with increasing fish size. Juvenile pollock generally selected the larger prey sizes relative to what was available. Juvenile pollock showed a marked preference for adult euphausiids and decapod larvae and an avoidance of copepods and chaetognaths relative to the numbers collected in net tows. These results are discussed relative to the feeding ecology of these juvenile fishes. This revised version was published online in July 2006 with corrections to the Cover Date.     

Dietary ratio of protein to carbohydrate induces plastic responses in the gastrointestinal tract of mice

Some vertebrates change the size of their digestive system in response to quantity and fibre content of ingested food, but the effects of dietary nutrients on gut structure remain poorly understood. Here we investigate how the protein to carbohydrate ratio of diets affects the mass of the gastrointestinal tract in mice. We fed 6-week-old male mice one of five isocaloric diets differing only in protein to carbohydrate ratio (the “no-choice” treatments), while a further four treatment groups received nutritionally complementary food pairings from which they could self-select a diet (the “choice” treatments). After 32 days, we measured the resulting dry mass of stomachs, intestines, caeca and colons. In the no-choice treatments, the stomachs were heavier in the mice fed diets containing more protein and less carbohydrate, indicating that larger stomachs may be needed for efficient digestion of the protein-rich food. In contrast, intestines, caeca and colons were heavier when diets contained more carbohydrates and less protein. This response may function to increase the digestive rate of carbohydrates when the dietary content of this macronutrient increases, but it may also indicate a compensatory response to increase amino acid uptake from a protein-deficient food. Mice in the choice treatments self-selected a diet with a protein to carbohydrate ratio of 0.46, and had gut dimensions similar to the expectation derived from no-choice treatments for this diet composition. Our results provide an example of plasticity in the differential allocation of resources to organ function, which is triggered by variation in resource quality.