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Feeding kinematics and performance of the endangered Rio Grande silvery minnow (Hybognathus amarus).

The Rio Grande silvery minnow (Cyprinidae: Hybognathus amarus) was at one time the most abundant fish in the Rio Grande and Pecos rivers occupying ca. 3,800 river km (2,400 miles) from the headwaters in Colorado through New Mexico and Texas to the Gulf of Mexico (Bestgen and Platania, 1991). Officially, H. amarus only occurs in the Middle Rio Grande of New Mexico, 280 km (174 miles) of river from Cochiti Dam to the crest of Elephant Butte Dam; this is ca. 7% of its former range. However, H. amarus is confined to an even smaller area between the diversion dam at Angostura and the San Acacia dam, a distance of 141 km, or ca. 3.7% of the former range of H. amarus. As a result, H. amarus was listed as endangered by the united States Fish and Wildlife Service (1994).

The Middle Rio Grande is generally characterized as slightly sinuous with straight, meandering, and braided reaches and a gravel riverbed downstream from Cochiti Dam and a shifting sand bed in the lower reaches (C. S. Crawford et al., in litt.). Dams on a large river should reduce turbidity downstream which in turn would increase the abundance of aquatic plants and shift the system toward the character of a mid-sized river (Ward and Stanford, 1983). While this may be the case for some rivers, the Middle Rio Grande is unique in that it regains turbidity downstream of Cochiti Dam to a mean turbidity of 20-1,200 nephelometric turbidity units through the reach at Albuquerque (D. Van Horn, pers. comm.). Moreover, penetration of light attenuates to zero at 30-40 cm minimizing or eliminating production of phytoplankton mid-river, and, consequently, benthic primary production is restricted to the shallow (10-20 cm) margins of the river and sand bars (Magana, 2007). Because of elevated turbidity, the feeding kinematics of fishes of the Middle Rio Grande have not been observed or documented.

Video-playback, digitally-modified video-images, and animations are powerful tools for exploring the interactions between morphological and behavioral components (Nicolette and Kodric-Brown, 1999). By analyzing data of video-taped animals, locomotor patterns and other typical behavior of a species can be accurately presented (Nicolette and Kodric-Brown, 1999). High-speed cinematography (>60 frames/s) is used extensively in elucidating rapid behaviors of fishes in semi-natural environments (Kodric-Brown, 1999). High-speed cinematography, coupled with imaging software, provides an invaluable tool for visualizing behaviors too fast to observe with conventional videography. Many feeding behaviors, particularly in larval animals, occur at speeds that exceed the resolution of conventional videography, but their visualization is crucial for a comprehensive understanding of a species. For example, cycles of feeding behaviors in fishes typically lasting 10-50 milliseconds (ms) which would only be captured in one or two frames of a conventional 30-Hz video-camera (Day et al., 2007). However, when filmed at higher speed (500 frames/s), it is possible to distinguish discreet feeding behaviors that would otherwise not be examined (Wintzer and Motta, 2005; Higham et al., 2006, 2007; Day et al., 2007).

Three principal feeding behaviors have been described for fishes. The majority of aquatic vertebrates are suction-feeders, by rapidly expanding the mouth cavity, they generate a flow of fluid outside the head to draw prey and small particles of food into the mouth through buccal suction (Ferry-Graham et al., 2003; Day et al., 2007; Bishop et al., 2008; Holzman et al., 2008). In fishes that employ suction-feeding, coordinating the timing of peak flow-velocity with opening of the mouth is important for successful capture of prey because forces are greatest on prey when the jaws are fully extended and the flow-field is at its largest (Holzman et al., 2007; Bishop et al., 2008). Other feeding behaviors include ram-feeding in which the fish overtakes the food (Wainwright and Ferry-Graham, 2001) and food-manipulation in which the fish dislodges food from a substrate or from a larger animal (Kislalioglu and Gibson, 1976; Osse, 1985). There is much literature on ram-feeding, suction-feeding, and capture of prey (Day et al., 2007; Higham et al., 2007); however, the process of feeding by benthic, freshwater fish on sessile prey remains understudied. Further understanding of the feeding behavior of benthic, freshwater fishes would provide insight into the feeding pressures and limitations of food a species may be experiencing under changing environmental conditions. The purpose of this study was to elucidate the feeding kinematics of the endangered H. amarus by determining how the species removes food from the substrate through buccal suction, biting the substrate, or both.

Materials and Methods--Because H. amarus is described as an herbivore (Whitaker, 1977; Sublette et al., 1999; Magana, 2009); samples with multiple species periphyton were collected from five sites located adjacent to the Middle Rio Grande north and south of Albuquerque, New Mexico. Samples of episammic (algae attached to sand) and epipelic (algae attached to rocks) periphyton were collected by pressing the top half of a Petri dish (100 by 15 mm) into the substrate and sliding a spatula underneath to remove the sample (Moulton et al., 2002). Each Petri dish was sealed with Parafilm[TM] (American Can Company, Greenwich, Connecticut) and transported to the United States Forest Service, Rocky Mountain Research Station (Albuquerque, New Mexico) for processing. Samples were washed into glass vials (0.5 dram) with Bozniak community growth media (Bozniak, 1969) and placed in three environmental growth chambers (10, 15, and 22[degrees]C at 10L:14D, 12L:12D, and 14L:10D photoperiods, respectively). Next, individual cells of diatoms were isolated from the washed samples and cultured in 50-mL Erlenmeyer flasks containing silica sand and Bozniak media. After visible algal growth (40-60 days) was present, cultured samples with <5% (determined by cell-counts) of nontargeted species of diatoms were saved as inoculums. Petri dishes containing growth media, agar, and sediment (Magana, 2009) were inoculated, and cultures were grown for 40-60 days. The resulting diatom-agar was used as the source of food for larval H. amarus during the study.

Larval H. amarus (ca. 200) used in this study were obtained from outdoor pools at the Albuquerque BioPark, Albuquerque, New Mexico. The larvae used were 2 weeks old and 9.0-14.4 mm in standard length. The collected larvae were transported to the Rocky Mountain Research Station Forestry Sciences Laboratory and placed into one 37.5-L aquarium where larvae acclimated to conditions of the laboratory for several days prior to filming (Higham et al., 2006). Sixty larvae were randomly selected; 10 of these were placed into each of six aquaria (37.5 L) for each filming event. All aquaria were maintained at room temperature (22[degrees]C) and a photoperiod of 12L:12D. To acclimate them to direct light, larval fish were exposed to a high intensity light (100W) prior to filming.

Over 3 days, ca. 150 high-speed (500 frames/s) digital video-recordings of H. amarus were made during the morning hours when the fish were most active. A Redlake Motionscope high-speed video-camera (Redlake, Tallahassee, Florida) was positioned ca. 75 cm in front of the aquarium prior to recording and focused on a 5-mm grid placed immediately behind the location of a piece (21 mm in diameter, 10 mm thick) of diatom-agar (Wintzer and Motta, 2005). The camera was set to record 4 s of motion at 500 frames/s (500 Hz; Wintzer and Motta, 2005; Higham et al., 2006, 2007; Day et al., 2007). The aquarium was illuminated from the front, and the three sides of the aquarium facing away from the camera were shielded to avoid any disturbance from movement in the background. Once the camera set up, a new piece of diatom-agar was placed into the aquarium in the same location as the previous one (Higham et al., 2006). After 5 min for fish to acclimate to the new source of food, feeding behavior of the fish was recorded at 4-s intervals until fish lost interest in the food. Each recording was saved and filed. The camera was then moved to the next aquarium for filming. After feeding behavior of H. amarus in the six aquaria was recorded, fish were removed. A new set of fish was placed in the aquaria and allowed to acclimate until the following day when the process was repeated. At the end of each day of recording, videos were reviewed for clarity and focus, and recordings of low quality were discarded. Although it was not possible to distinguish between individual larvae in each aquarium, the use of six aquaria in rotation and exchange of larvae between filming days assured that as many different larvae as possible were filmed to avoid pseudoreplication (Wintzer and Motta, 2005). In most instances, multiple animals were feeding on the piece of diatom-agar at the same time, and an effort was made to film as many larvae as possible (Lachlan et al., 1989; Brown and Laland, 2001). After review of video footage, 49 recordings containing 302 feeding cycles were saved. Video recordings were viewed first in Quicktime Pro 7.0 and shortened to only include the approach and feeding sequences (ca. 240-2,000 frames/event). An effort was made to select from a variety of different recordings to ensure that the analysis would include as many larvae as possible.

Approach and feeding angles were analyzed with ImageJ (ImageJ version 1.44p; W. Rasband, National Institutes of Health, http://imagej.nih.gov/ij). Although the camera was positioned 75 cm in front of each aquarium, the flexibility of Image J software gave the advantage of zooming into each image up to 800%, analyzing feeding kinematics frame by frame, and measuring with a high temporal (2 ms, ca. 500 frames/s) and spatial (<1 mm) resolution for each feeding sequence (Day et al., 2007). Pearson's product-moment correlations (SAS version 9.3, Corr Procedure, SAS Institute Inc., Cary, North Carolina) was used to determine the relationship among five performance variables: duration (seconds), amount of time the individual fish hovered over the piece of diatom-agar while touching, tasting, or feeding; approach angle, orientation of the long axis of the fish when coming into the field of view; feeding angle, orientation of the long axis of the fish with respect to the surface of the piece of diatom-agar to touch, taste, or feed; touches, the fish touches the substrate, then rises, and opens its mouth with or without buccal action; bites, the fish touches the substrate, then bites, and terminates with buccal action.

To quantify feeding kinematics, anatomical landmarks were measured on each image of a fish in each frame of video. The selection of points varied according to the axis of the body in view. Peak opening of the jaw, depression of the hyoid bone, protrusion of the premaxilla, lateral movement of the head, and buccal velocity were measured. All variables of feeding kinematics were measured in millimeters and degrees using the line-and-angle tool in ImageJ (Wintzer and Motta, 2005). Peak opening of the jaw (gape) was measured by identifying and manually measuring the distance between the tip of the premaxilla and the mandible. Maximum depression of the hyoid bone was measured from the dorsal edge of the head across the center of the eye to the bottom of hyoid bone. Protrusion of the premaxilla was measured from the ethmoid bone to the tip of the extended premaxilla. Rapid lateral movements of the head were analyzed from videos with dorsal views and were measured on same side of the head from the beginning of movement on the outside edge of the head until the brisk sweep was complete. The x-y position of each was used to calculate each kinematic variable using Microsoft Excel spreadsheet (Day et al., 2007). Pearson's product-moment correlation was used to evaluate feeding kinematics of duration and maximum gape. Data were checked for outliers, and Tukey's rule of 1.5 times the interquartile range beyond the firest or third quartiles was used for all data except that for particles for which Dixon's test was used due to small sample size.

RESULTS--Although a maximum of 500 frames/s was used to record feeding behavior, some feeding kinematics exceeded the display speed of the software (0.01 s) and could only be analyzed frame by frame (one frame = 0.002 s). Larval H. amarus arrived at the food source using their pectoral fins for braking, maneuvered, and assumed a 24-90[degrees] position above the food. Posture of the body of H. amarus when feeding was the typical fast-start S-shape of piscivorous fish (Domenici and Blake, 1997; Wintzer and Motta, 2005). Results of feeding kinematics are outlined in Table 1. Results from correlation analysis indicate that duration and touches as well as duration and bites were highly and significantly correlated at 0.74 (P < 0.001) and 0.62 (P < 0.001), respectively, while touches and bites were less correlated but statistically significant at 0.54 (P = 0.002).

Analysis of video showed two types of feeding movements in this highly dynamic fish. In the first feeding movement, H. amarus approached the substrate at 30-60[degrees], touched the substrate with mouth closed, rose (1-3 mm), opened its mouth, and repeated the process two or three times with no obvious attempt to bite into the substrate before moving elsewhere. With each rise and opening of the mouth, H. amarus tasted food to determine quality of food. This feeding movement is detailed in Fig. 1. The elapsed time for tasting sequences was ca. 50 ms.

The second feeding movements observed were actual feeding sequences whereby larvae bit into substrate and terminated the feeding sequence with a rapid lateral movement of the head (Fig. 2). The sequence of movements of the jaw during feeding by H. amarus was as follows: 1) approached the food in a manner similar to that in the tasting sequence except that H. amarus took a more vertical position (ca. 80-95[degrees]) to substrate; 2) touched substrate and rotated to 90[degrees]; 3) began opening mouth; 4) achieved peak opening of the jaw (0.01 s) and premaxilla swung anteriorly; 5) mouth began closing and maximum depression of the hyoid achieved, synchronized with buccal action; 6) mouth closed and premaxilla retracted to normal position. Elapsed time for this feeding sequence was 80 ms.

[FIGURE 1 OMITTED]

Utilization of suction during capture of prey was estimated rather than empirically measured (Wainwright et al., 2001). Although diatoms are much too small to observe in the videos, buccal velocity was calculated by carefully observing ingestion of particles (0.18-0.22 mm) by H. amarus. The translucent nature of 2-week old larvae of H. amarus facilitated ventral viewing of particles moving from the substrate into the larvae and past pharyngeal teeth. Buccal velocity was calculated by measuring distance and time of particles ingested (Fig. 3). Mean buccal velocity was 82 mm/s [+ or -] 1.5 (n = 3). Regurgitation of food by H. amarus also was observed, and velocity of regurgitation was calculated at 25 mm/s (Fig. 4).

DISCUSSION--The results from this study of feeding performance indicate that H. amarus is a visual and tactile feeder. This study also indicates that H. amarus can recognize sources of food after a brief learning period and will feed until satiated or until the food is exhausted. It may be unusual for multiple fish to feed on the same piece of food simultaneously, but, in laboratory settings, H. amarus usually feed in groups. When one H. amarus found a preferred species of diatoms, cohorts came and fed as a group. Magana (2009) found that H. amarus is an effective social learner (Lachlan et al., 1989; Suboski and Templeton, 1989; Brown and Laland, 2001, 2003) and can be taught to feed on pieces of diatom-agar after one brief exposure of 30 min.

Vision is the dominant sense in many fishes and can be predicted by the large size of the eyes of species in which vision dominates (Rowland, 1999); yet turbidity in the Rio Grande may inhibit the ability of H. amarus to see food in its natural environment, which would require use of other sensory organs to locate food. Scanning electron microscopy of larval H. amarus showed that the inside and outside of the mouth are covered with putative taste papillae (taste buds). in fish, taste buds are not only within the oral cavity, pharynx, esophagus, and gills but also may occur on the lips, barbells, and fins and over the entire body surface in many species (Gomahr et al., 1992; Bouriot and Reutter, 2001; Kasumyan and Dving, 2003; Dieterman and Galat, 2005; Devitsina, 2006). Gomahr et al. (1992) reported that minnows had the highest density of taste buds in the gular region (297/[mm.sup.2]) and on pectoral fins (138/[mm.sup.2]). The external taste buds are thought to be specialized for searching for food and discrimination of amino acids (Kotrschal, 2000). Kasumyan and Dving (2003) have suggested that extraoral taste systems are 10 times more sensitive than the oral system. Hence, these taste papillae may provide sufficient tactile stimulation for H. amarus to locate and discern food in conditions of low or no visibility.

[FIGURE 2 OMITTED]

A review of the literature on feeding kinematics shows most research has been conducted on species of midwater fishes that employ ram-feeding where they pursue elusive prey and feed at speeds from 10-50 ms (Bence, 1986; Brown and Laland, 2001; Wintzer and Motta, 2005; Higham et al., 2006, 2007; Day et al., 2007; Holzman et al, 2007). In contrast, H. amarus is a benthic feeder feeding on sessile prey, yet their feeding speeds also are very rapid at 50-80 ms.

Whether piscivorous or herbivorous, fishes employ the same suction-feeding mechanism for capture of prey by synchronizing opening of the mouth, depression of the hyoid, and opercular expansion to create a flow of water into the mouth (Day et al., 2007; Bishop et al., 2008). The rapid expansion of the buccal cavity produces high fluid velocities and accelerations that extend only a short distance from the mouth (approximately one half of the diameter of the mouth), and only persist for several milliseconds (Bishop et al., 2008; Holzman et al., 2008). The size of this region varies in direct proportion to the diameter of the mouth throughout feeding (Day et al., 2007). Coordinating the timing of velocity of peak flow with opening of the mouth is important for capture of prey because higher forces are exerted on prey when the jaws are fully extended and the field of flow is at its largest (Bishop et al., 2008).

Buccal velocity has been investigated thoroughly with various species of piscivorous fish (Wintzer and Motta, 2005; Higham et al., 2007; Bishop et al., 2008) and timing of velocity of peak flow is key for piscivorous fishes (Holzman et al., 2007). Therefore, the predator must precisely time its strike to locate the prey within the narrow region of high flow, during the brief period when flow is at its peak (Holzman et al., 2007). In contrast, H. amarus does not have a strike-timing constraint, yet it feeds at speeds approaching those of piscivorous fishes. Piscivorous and herbivorous fishes use buccal action to draw prey into their mouths; however, if the prey is securely attached to the substrate, a higher force is required to detach it (Denny et al., 1985). Hybognathus amarus also uses a rapid lateral movement of the head to detach food from substrate. Closer examination revealed that the lateral movement of the head was related to the detachment of filamentous algae from the substrate. Day et al. (2007) reported that some species of fish have small mouths and hold their body still while drawing the prey into their mouths. While H. amarus have a small mouth, they do not hold their body still while feeding. Closer inspection of H. amarus revealed that its body is in constant motion while actively feeding.

[FIGURE 3 OMITTED]

The feeding mechanism of teleosts is characterized by an extreme anterior swing of the premaxilla and rapid depression of the hyoid occurring synchronously with the closing of the mouth (Lauder, 1979). The extreme anterior swing of the premaxilla ensures peak opening of the jaw; however, in H. amarus, the premaxilla does not reach maximum protrusion and depression of the hyoid until after the jaws have begun to close. The sequence of jaw-opening and hyoid-depression in H. amarus is similar to that reported for Amia calva (Lauder, 1979) in that depression of the hyoid is not synchronized with opening and closing of the mouth. Hybognathus amarus is similar to A. clava, in that the opening of the mouth occurs rapidly and the distance between the jaws reaches its maximum within 0.01 s.

[FIGURE 4 OMITTED]

Bence (1986) reported that individual Gambusia affinis selected the most profitable Ceriodaphnia dubia (Cladocera) over less profitable cyclopoid copepods to a greater degree after being exposed to both types of prey rather than individual experiences with only one type of prey. Magana (2009) reported that H. amarus will eat diatoms with erect form of growth, considered food of good quality with a proportionally small amount of biogenic silica and agar-substrate to a relatively large amount of organic matter. The opposite scenario is true for prostrate forms of growth, which are considered food of poor quality because an aquatic grazer must deal with a relatively large portion of indigestible biogenic silica and substrate to gain a proportionally small amount of organic matter. Observed feeding behavior of H. amarus revealed that, when food of lesser quality is consumed, the individual fish will regurgitate food in its mouth (Fig. 4).

Hybognathus amarus has evolved a feeding behavior to cope with a turbid environment. However, the question of why they feed so fast remains. In a turbid environment, the rates of encounter with prey can be limited; therefore, H. amarus must be quick to assess quality of food and feed before losing physical contact.

Many thanks are extended to M. Julius and H. Schoenfuss for their help with scanning-electron-microscopy imaging and high-speed video-filming. I also thank B. Zimmerman, D. Price, and A. Muldoon for their work on the isolation of diatoms and to T. Perez and her staff at the Albuquerque BioPark for their assistance with collecting Rio Grande silvery minnows used in this study under United States Fish and Wildlife Service permit TE097324-0 to HAM.

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Submitted 5 August 2012. Acceptance recommended by Associate Editor Robert J. Edwards 18 February 2013.

HUGO A. MAGANA

United States Department of Agriculture Forest Service, North Fork John Day Ranger District, 401 West Main Street, Ukiah, OR 97880

Correspondent: hmagana@fs.fed.us
TABLE 1--Feeding kinematics of Hybognathus amarus with results
of analysis for outliers.

Parameter                         n      Mean [+ or -] SE     Minimum

Peak jaw-opening time (s)         45   0.019 [+ or -] 0.002    0.01
Peak jaw-opening size (mm)        45    0.34 [+ or -] 0.013    0.01
Premaxilla protrusion (mm)        16    0.28 [+ or -] 0.12     0.20
Premaxilla protrusion time (s)    16   0.018 [+ or -] 0.003    0.01
Lateral movement of head (mm)      7    1.18 [+ or -] 0.13     0.50
Lateral movement of head (s)       7    0.02 [+ or -] 0.002    0.01
Hyoid depression (mm)             16    0.16 [+ or -] 0.011    0.05
Hyoid depression time (s)         16    0.02 [+ or -] 0.002    0.01
Buccal velocity (mm/s)             3    82.0 [+ or -] 14.5    53.0
Regurgitating (mm/s)               3    23.9 [+ or -] 2.0     20.0
Regurgitating time (s)             3    0.03 [+ or -] 0.003    0.03

Parameter                         Maximum   Potential
                                             outliers

Peak jaw-opening time (s)          0.05     None
Peak jaw-opening size (mm)         0.38     None
Premaxilla protrusion (mm)         0.35     None
Premaxilla protrusion time (s)     0.04     0.04
Lateral movement of head (mm)      1.50     0.50
Lateral movement of head (s)       0.03     0.01, 0.03
Hyoid depression (mm)              0.25     0.05
Hyoid depression time (s)          0.04     0.04
Buccal velocity (mm/s)            98.0
Regurgitating (mm/s)              26.7
Regurgitating time (s)             0.04
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