FEEDING MORPHOLOGY AND KINEMATICS IN SURFPERCHES
(EMBIOTOCIDAE: PERCIFORMES): EVOLUTIONARY
AND FUNCTIONAL CONSEQUENCES
A Thesis Presented to the Faculty of California State University, Stanislaus and Moss Landing Marine Laboratories
In Partial Fulfillment of the Requirements for the Degree of Master of Science in Marine Science
By Kimberly Quaranta June 2011
i
ACKNOWLEDGEMENTS
This work would not have been made possible without the acceptance, battle,
forgiveness, and mentorship of Dr. Lara Ferry. She helped create a love for functional morphology and fishes, and gave me a chance when needed most. To Dr. Greg
Cailliet, who in his own right is a gift to life learning, I am truly grateful to have worked on this thesis with him. It has been an academic and emotional adventure that has left me a better person due to his influence and guidance. Dr. Peter Wainwright was instrumental in providing valuable comments and time spent pouring over my dataset. This thesis or dream of becoming a marine scientist would also not have been possible without the amazing support of Dr. Pam Roe. Gratitude for her efforts in processing paperwork, valuable edits and comments, and overall passion and enthusiasm for science will never fully be adequately expressed in words. To all my friends and cohorts at MLML for countless hours working late nights, playing foosball, having wonderful dinner parties, scuba diving, helping each other with our research, and just being there for one another, I thank you. To all the MLML staff and faculty, you truly made this experience special and unforgettable. Special thanks to
Kenneth Coale, who has been a great leader, friend and teacher. Lastly, I would like to thank my family. My mother, Carol and father, Joseph for giving me life, and everything I could have ever wanted from it.
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TABLE OF CONTENTS PAGE
Acknowledgments…...... iii
List of Tables ...... v
List of Figures...... vi
Chapter I Abstract...... 2 Introduction...... 4 Methods...... 7 Results...... 11 Discussion...... 14 References...... 25
Appendix I: Morphological and mechanical characteristics of the body and feeding apparatus in 10 species of embiotocids...... 56
Chapter II Abstract...... 59 Introduction...... 61 Methods...... 64 Results...... 66 Discussion...... 67 References...... 73
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LIST OF TABLES
TABLE PAGE
Chapter I
1. Location and method of collection for surfperch specimens...... 33
2. Principle components analysis on 10 morphological variables related to feeding in 10 embiotocid species...... 34
3. One way Analysis of Variance (ANOVA) for each PCA explaining 10% or more of the total variance...... 35
TABLE PAGE
Chapter II
1. Measurements made to produce kinematic variables (Westneat, 1990)...... 82
2. Mean peak maximums and standard error for all five kinematic variables measured during high speed video ...... 83
3. Mean time to peak maximums and standard error for all five kinematic variables measured during high speed video ...... 84
4. Results of t values for differences amongst Embiotoca jacksoni and Embiotoca lateralis for each kinematic variable ...... 85
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LIST OF FIGURES
FIGURE PAGE
Chapter I
1. Head length, standard length, and total length measurements made ...... 37
2. Diagram showing depression of the lower jaw resulting in protrusion of the upper jaws...... 38
3. Illustration of vertical and horizontal gape measurement...... 39
4. Placement of the adductor mandibular and sternohyoideus ...... 40
5. Placement of the levator posterior muscle and lower pharyngeal jaw plate in embiotocids ...... 41
6. Lower jaw levers for calculating mechanical advantage ...... 42
7. Measurements of the four links used in calculating the kinematic transmission coefficient ...... 43
8. Separation of embiotocid species along PC 1 (26.8 %)...... 44
9. Boxplot of the adductor mandibulae mass...... 46
10. Boxplot of vertical gape...... 47
11. Boxplot of the sternohyoideus muscle mass...... 48
12. Boxplot of jaw opening mechanical advantage ...... 49
13. Boxplot of the kinematic transmission coefficient (KT) for the oral four-bar linkage mechanism ...... 50
14. Separation of embiotocid species along principle component axis 3 (17.8 %)...... 51
15. Boxplot of the variable, levator posterior muscle (A), which loaded highest on principle component 3 and the lower pharyngeal jaw mass that loaded next highest ...... 52 vi
16. Separation of embiotocid species along PC 4 (12 %)...... 53
17. Box plot of the highest loading variable, jaw closing mechanical advantage, on principle component axis four ...... 54
FIGURE PAGE
Chapter II
1. Landmarks associated with measurements made for all kinematic variables, from Westneat, 1990...... 87
2. Still frames from high speed video showing prey capture and expression of kinematic variables...... 88
3. Strike patterns for Embiotoca jacksoni and Embiotoca lateralis...... 89
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CHAPTER ONE
ANALYSIS OF THE TROPHIC MORPHOLOGY AND MECHANICS IN 10
SPECIES OF SURFPERCHES (PERCIFORMES: EMBIOTOCIDAE)
1
ABSTRACT
The surfperch family (Embiotocidae) is relatively small, having 23 species and occupying temperate water. They exhibit highly derived jaw morphology resembling that of tropical species, such as labrids, with tremendous diversity. Surfperches forage in specific, often predictable ways, and can be categorized into winnowers, pickers
(nonwinnowers), and crushers. In addition, surfperches are viviparous and lack larval stages thus limiting their distribution. Therefore, it is hypothesized that their jaw morphology has led to their success in partitioning resources by means of their foraging behavior. This study used morphometrics to assess the potential diversity in
jaw morphology among 10 species in this family. Measurements were made on
preserved specimens, including jaw lengths and mass of muscles associated with
operation of the jaw. The large set of morphometrics was analyzed using a Principal
Components Analysis to determine which variables explained the most variation in
surfperch jaw morphology and diversity, in addition to an Analysis of Variance
(ANOVA) to determine how they differ from one another. The morphology of
surfperches did not differentiate between pickers and winnowers, but morphology
was able to distinguish the one species noted as a crusher (Damalichthys vacca).
However, the data showed that there were significant differences among species in
jaw morphology and musculature. Although there was not a direct correlation
between foraging behavior and morphology, it is likely that surfperches coxist based
2
on their ability to modulate prey acquisition in their habitat. Despite the relatively low number of species within this family, it is likely that the adaptive potential is developing within this group. Therefore, morphology of the feeding apparatus in surfperches is different among species to better suit environmental circumstances
(microhabitat and prey acquisition) under continuous selection pressures such as availability of new prey or competition for current prey, resulting in more definitive foraging behaviors in the future.
3
4
INTRODUCTION
The family Embiotocidae includes a group of fishes distributed mainly along the coastline of the eastern North Pacific Ocean. Of the 23 species that make up this family, 20 occur along the coast of North America, while two species inhabit waters of Japan and one species is entirely fresh water (Bernardi & Bucciarelli, 1999). One of the most distinctive characteristics this family possesses is the ability to give birth to live young. Many other teleosts are oviparous and lay millions of eggs that develop into larvae in the ocean. These larvae are transported in the top layers of the water column and can be distributed relatively great distances by ocean currents.
Surfperches do not have this dispersive life stage and are born and remain in close proximity to their parents, and those of other species in that habitat. Therefore, many species co-occur in similar habitats, resulting in the potential sharing of food and spatial resources and the possibility of competition.
Surfperches show a remarkable degree of resource partitioning that includes both generalists and extreme specialists that tend to occur sympatrically with other members of this family, partly due to the localized nature of viviparity. Several studies have attempted to explain the feeding morphology observed within the embiotocids, with much focus centered on the interactions between two closely related species, Embiotoca lateralis and Embiotoca jacksoni (Alevizon, 1975; Hixon,
1980; Schmitt & Coyer, 1982, 1983; Schmitt & Holbrook, 1984; Holbrook &
Schmitt, 1986). E. lateralis and E. jacksoni are congeners that live coastally and in sympatry along much of the California coast with extensive dietary overlap (Hixon, 5
1980; Schmitt & Coyer, 1982). It has been suggested that these two species can co- inhabit areas by utilizing differences in foraging behavior and microhabitat selection
(Schmitt & Holbrook, 1984). This is primarily achieved by E. jacksoni’s ability to winnow prey items from less profitable habitats in the presence of E. lateralis
(Schmitt & Coyer, 1982). Similarly, differences in the pharyngeal jaw dentition and musculature between Rhacochilus toxotes and Damalichthys vacca (formerly congeners) enable this pair of closely related species to utilize different food items and coexist in same habitats (Alevizon, 1975).
A difference in how a fish eats (i.e., the ability to capture and process prey) has been suggested to be more important than what a fish eats (Motta, 1988).
Historically, the classification of feeding guilds is determined by prey choice, such as herbivory, piscivory, and planktivory. However, the morphology itself should constitute structures related more to the way food is collected (or processed) than to the food type itself, for example oral shelling or pharyngeal crushing of molluscs
(Motta, 1988). For surfperches, these guilds have been dubbed “picker, winnower and crusher” (Laur & Ebeling, 1983). However, morphological comparison among these three types is difficult since winnowing and crushing of hard-shelled invertebrates is a primary function of the pharyngeal jaw apparatus and the category picking is inherently a function of the oral jaws, which are also involved in suction feeding.
Fundamentally, how fish procure food can be defined and divided into two categories: 1) those that rely on the activity of the oral jaws, such as suction feeding, ram feeding, and biting; and 2) those that rely on features of the pharyngeal jaws and 6 other organs derived from the gill arches, such as suspension feeding and prey processing with pharyngeal jaws (Horn & Ferry-Graham, 2006). Of the three types of surfperch foraging behaviors mentioned above, pickers fit into category one, with winnowers and crushers fitting into both one and two. However, it is interesting that pickers may also possess the same morphology as those species that actively winnow but have only been observed to visually locate and utilize suction in capturing prey with little processing from the pharyngeal jaws (Laur & Ebeling, 1983; Ebeling &
Laur, 1986).
Species commonly do not utilize the same array of prey as their close relatives, but rather a distinct subset, or entirely different set of prey (Ferry-Graham,
Bolnick, & Wainwright, 2002). However, surfperches are not only closely related and have recently speciated, but also overlap significantly in habitat occupation and therefore prey utilization as well (DeMartini, 1969; Ellison, Terry, & Stephens,
1979). These ecological perspectives along with the life history of this family and unique pharyngeal jaw morphology make the Embiotocidae a rich prospect for a functional morphological study of feeding mechanisms. This study attempted to answer the following two questions relating to feeding morphology and patterns of behavior and resource use: 1) do surfperches have distinct feeding morphologies that correlate to specific foraging behaviors (Laur & Ebeling, 1983); and 2) to what extent does feeding morphology vary among the species being studied?
7
METHODS
Feeding Morphology and Mechanics
The feeding morphology and mechanics were obtained from several species within the family using the methods outlined below. Location, numbers, and species used in this study are listed in Table 1. Specimens were collected using trawls, beach seines, scuba, and spear fishing with permission of the California Department of Fish and Game (permit # 816403) and in accordance with San Jose State University
IACUC protocol 814. Specimens were fixed in a 10% buffered formalin solution and then transferred to 70% ethanol for storage. Specimens were weighed (after preservation and rinsed in water) and morphological measurements of the external anatomy of specimens were taken using calipers to the nearest tenth millimeter (mm) or measuring tape to the nearest mm and followed Cailliet, Love, & Ebeling, (1986).
These included total length, TL (cm); standard length, SL (cm), and head length,
HDL (mm) (Figure 1). Other variables were collected via physical depression of the lower jaw until maximum extension (without forcing) such that jaw protrusion, vertical mouth gape, and horizontal mouth gape could be measured. These measurements follow Wainwright, Bellwood, Westneat, Grubich, & Hoey, (2004) and are denoted as follows (and shown in Figure 2): 1) jaw protrusion, the excursion distance of the anterior symphysis between the two premaxillae as they travel rostrally when the jaws are protruded; 2) vertical mouth gape, the vertical distance from the center of the upper jaw to the center of the lower jaw in an opened position; 8 and 3) horizontal mouth gape, the horizontal distance between the coronoid process of the articular bones inside the opened mouth (Figure 3).
Muscles associated with feeding were removed and weighed for each fish.
This included all of the sections of the adductor mandibulae (AM) except for Aw, which are a complex of muscles used to adduct the jaws, forcing it closed. In
th addition, the levator posterior (LP)/4 and levator externus (LE4) were also removed.
These are the muscles responsible for the adduction of the pharyngeal jaws. Finally,
the sternohyoideus (SH), which is the primary muscle that abducts the lower jaw, was
also weighed. Wainwright (2004) characterized the origin and insertion of the
adductor mandibulae and sternohyoideus muscles in labrid fishes. The AM (Figure
4A) originates broadly from the lateral surface of the suspensorium and attaches
directly to the articular and by tendons to the maxilla and articular bones and the SH
(Figure 4B) originates on the anterior surface of the ventral region of the cleithrum
bone and ventrally is continuous with slips of the hypaxial musculature until it
attaches on both sides of the urohyal bone (which is removed in addition to the
muscle) (Wainwright, et al., 2004). The LP (Figure 5) originates from the ventral
aspect of the pterotic to insert tendinously on the posterolateral corner of the fourth epibranchial muscle. The LE4 is the only muscle in the composition of a “muscular
sling,” ventrally inserting tendinously on the lateral margin of the fourth epibranchial, but most of the fibers continue their course beyond epibranchial 4 to fuse with the central head of the obliquus posterior (Liem, 1986). In addition, the complete lower 9 pharyngeal jaw plate (Figure 5) was removed and cleaned of any tissue to obtain a dry weight.
Several traits were measured that reflect the mechanical properties of the oral jaws. These traits were used to construct biomechanical models allowing for collection of quantitative data that represent the functional morphology of feeding in these fishes. The simpler of the two models employed in this study use lever ratios associated with opening and closing of the lower jaw and are based on the engineering theory of levers and linkages (Westneat, 1990). Velocity and force transmission can be quantified by calculating mechanical advantage. Mechanical advantage is the ratio of the force applied to a load, to the force applied by the effort
(McGowan,1999). Lever systems used in jaw mechanics support a tradeoff between force and velocity transmission, in that species with high values for this variable have jaws modified for force, whereas, species with low values can open their jaws more quickly. Calculation of lower jaw levers and mechanical advantage followed
Westneat (1995). For jaw closing and opening, the lower jaw out-lever was the distance from the tip of the mandible to the quadrate-articular joint (Figure 6). Jaw opening in-lever was the distance along the articular from the insertion of the interoperculomandibular ligament to the quadrate-articular joint and jaw closing in- lever was the distance from the insertion of the adductor mandibulae muscle on the coronoid process to the quadrate-articular joint (Figure 6). To calculate mechanical advantage (MA), the ratio of in-levers to out-lever was used:
10
MAjaw opening = jaw opening in-lever / jaw out-lever
MAjaw closing = jaw closing in-lever / jaw out-lever
The more complex model incorporated multiple levers and linkages and is
called the “anterior jaws four-bar linkage mechanism” (Westneat, 1990). The anterior
jaws four-bar linkage estimates the transfer of motion to the maxillary for the purpose
of protruding the premaxilla forward (Westneat, 2004). A kinematic transmission
(KT) coefficient can be calculated as the ratio of output motion to input motion of the
linkage (Westneat, 1995). Similar to the jaw-opening lever system, maxillary KT also
possesses the tradeoff between force and velocity modified. Four links (fixed,
coupler, output, and input) composing the linkage and the diagonal were measured on
the fish in a relaxed state with the jaws closed (Figure 7). The following descriptions
of these links will follow Wainwright (2004), modified from Westneat (1990). The
fixed link is the distance between the quadrate-articular joint and the proximal base of
the nasal bone; the coupler link is the distance from the proximal base of the nasal bone to the distal end of the nasal bone at its ligamentous connection to the maxilla; the output link is the distance from the distal end of the nasal to the confluence
between the distal end of the alveolar arm of the premaxilla, the distal arm of the
maxilla and the coronoid process of the mandible; the input link is the distance
between the latter joint just described and the quadrate-articular joint.
11
Statistical Treatment
A Principal Components Analysis (PCA) was performed using all morphological variables measured. The PCA creates new variables of PC scores that are uncorrelated to each other and scored according to the amount of variation explained in the original data. The principal components (PCs) were then used to analyze if differences existed among variables using a Multivariate Analysis of
Variance (MANOVA). Given significant MANOVA results, Analysis of Variance
(ANOVA) was conducted with a post-hoc multiple comparisons test using least- significant differences (LSD) to determine how each species differs.
Other statistics employed in this study (but results were omitted as they offered no new information) included the evaluation of Independent Contrasts using the free software of Mesquite, version 2.01. The results obtained from this analysis showed that phylogenetic relationships did not account for differences seen in morphology of this particular group of fishes. Therefore, only the raw morphological data were used in the analyses. In addition, corrections for size were made prior to running the PCA analysis. This was performed to avoid having all the variables be highly correlated. Therefore, it was subjected to further testing per the conditions of the PCA.
RESULTS
This analysis of the feeding morphology in 10 species of embiotocids revealed significant differences among members of this family. The PCA (Table 2) generated 12 four new PCs resulting in eigenvalues greater than one and accounted for 77.4% of the variation within the morphological data set (Appendix I). Since MANOVA
(multivariate analysis of variance) results showed significant differences for all principal components (P < 0.01), an analysis of variance (ANOVA) was performed on each principal component to determine post hoc where differences occurred between species (Table 3) using a multiple comparison test (Fisher’s LSD) for each
ANOVA.
The first two principal components accounted for almost half of the variation
(47.6%) seen in feeding morphology among surfperch. The variables that loaded most heavily on PC 1 included adductor mandibulae mass, sternohyoideus mass, and vertical gape. These variables relate to how large the mouth is opened and the muscles that operate that movement. Therefore, a large vertical gape requires large jaw opening and closing muscles. Those species that loaded high on PC 1 were
Amphistichus argenteus, Embiotoca jacksoni, Zalembius rosaceus, and Damalichthys vacca (Figure 8A). Amphistichus argenteus and E. jacksoni loaded the highest and are significantly different from the other members of the family, and both had the highest values for adductor mandibulae mass (Figure 9). Amphistichus argenteus also showed incredible diversity in vertical gape. It had a 118% difference in vertical gape compared to that of the next largest gape seen in Rhacochilus toxotes (Figure 10).
Embiotoca jacksoni had the largest sternohyoideus muscle mass and was the only species significantly different from all the other species (Figure 11). 13
Principal component 2 loaded most heavily and negatively for jaw-opening mechanical advantage, and loaded positively for maxillary KT (Figure 8B). Species that loaded strongly on the axis for force-modified jaws included Embiotoca jacksoni,
E. lateralis, and Hypsurus caryi. With the exception of Rhacochilus toxotes, these three species exhibited the highest values obtained for jaw-opening mechanical advantage (Figure 12). Consequently, those species that loaded for velocity modified jaws (high PC 2 scores) included Damalichthys vacca, Cymatogaster aggregata, and
Amphistichus argenteus. Cymatogaster aggregata possessed the most velocity- modified jaws and this species had a statistically different jaw-opening mechanical advantage (Figure 12). However, D. vacca and A. argenteus might be more influenced by other variables that also loaded high on PC 2 but less than 0.6, as neither of them had extreme values for jaw-opening mechanical advantage (Figure
12). High PC 2 values also resulted in species with high maxillary KT. Embiotoca jacksoni and E. lateralis had low maxillary KT values and were therefore, forced modified (Figure 13). Cymatogaster aggregata had the highest maxillary KT value and also loaded high in PC 2.
Principal component 3 had a very distinct variable (the levator posterior muscle) that loaded highest and accounted for 17.8% of the variation. The levator posterior muscle is responsible for adducting the pharyngeal tooth plate. The one species that loaded heaviest on PC 3 was Damalichthys vacca (Figure 14). This species is unique among embiotocids in the pharyngeal tooth plate and associated musculature. Values recorded for D. vacca were significantly different from all 14 species in this study, and 93% different for the levator posterior muscle mass and
98% for the lower pharyngeal tooth plate (Figure 15). In addition to D. vacca,
Zalembius rosaceus and Amphistichus argenteus were the next closest species with large levator posterior muscle mass and lower pharyngeal tooth plate mass (Figure
15). However, this significant result in their morphology was not a determining factor for PC 3, as both species loaded significantly less than D. vacca and other species
(Figure 14).
The last principal component (PC4) accounted for 12 % of the variation and had only one variable that loaded highly: jaw-closing mechanical advantage.
Rhacochilus toxotes loaded the highest on PC 4 followed by Amphistichus koelzi, A. argenteus, Embiotoca lateralis, and Damalichthys vacca (Figure 16). Those species that had more forced modified jaws include A. koelzi, R. toxotes, and D. vacca
(Figure 17). However, like Cymatogaster aggregata, E. lateralis and A. argenteus had more force-modified jaws (Figure 17) but loaded high on PC 4, meaning that jaw-closing mechanical advantage is not as important in characterizing their feeding morphology.
DISCUSSION
This study focused on morphological differences in the jaw features among 10 embiotocid species. The morphological data suggest that there is indeed a significant difference among species of surfperches with regard to their feeding morphology
(Table 3), and that these differences most likely have ecological implications. 15
DeMartini (1969), characterized and documented the mouth and tooth morphology of all 23 extant species of surfperches. His conclusions stated that, as a group, embiotocids can be mainly classified as benthic grazing carnivores feeding on crustaceans. While this is true, feeding morphology analyzed in this study suggest that the diverse jaw morphology of these species lends to more disparate classifications. Each species examined exhibited an extreme quality in one or more of the variables. These differences suggest that their morphology allows for a wider range of feeding behavior, or that each species is becoming more specialized to a particular habitat or prey choice. Relating these species-level differences to aspects in the overall ecology of surfperches is challenging given that foraging patterns observed in past studies do not correlate with patterns of feeding morphology documented here.
Feeding morphology and foraging behaviors
Two of the three foraging patterns (which include both procurement and processing) observed in past studies (winnowing and picking) were not distinguished by the data gathered in this study. The third foraging type, crushing, was detected through morphological variables associated with feeding structure and musculature.
This type of foraging is accomplished only through extreme hypertrophy within the feeding apparatus. Therefore, detectable differences were observed in the data for
Damalichthys vacca, the only crusher. However, although no distinction was made between winnowing and picking, analyses of the variables resulting in PCA plots 16 show the separation of all species in morphospace for feeding morphology and mechanics (Figures 8, 14, 16).
Morphological variation among individuals may influence foraging efficiency, and the ability of an individual to utilize a particular prey array in a specific habitat.
According to Laur and Ebeling (1983), Embiotoca Jackson, Embiotoca lateralis,
Hypsurus caryi, Rhacochilus toxotes, and Damalichthys vacca comprise a feeding guild (similar in that they continually seek small prey hiding in benthic turf), in which each species can therefore coexist on the same reef. Data in their study showed differences in diet, foraging behavior and microhabitat use. It was their conclusion that each species selected food in fundamentally different ways as a result of their foraging behavior (Laur & Ebeling, 1983). This information was then used to distinguish species as “oral winnowers” (E. jacksoni, H. caryi, and R. toxotes) or
“nonwinnowers” (E. lateralis and D. vacca) based on the percent of total bites with casts (rejected material that is expectorated). They did not measure any feeding structures that might support why each species foraged in a separate way. If these individuals have fundamentally different ways in which they choose prey, then their underlying morphology should support foraging behavior observed – winnowing versus non-winnowing. However, according to the data presented here, feeding morphology for these five species is highly variable, making it difficult to establish a strong relationship between foraging behavior observed by Laur & Ebeling (1983) and their underlying morphology. 17
Similar conclusions were drawn in a subsequent study of the same surfperch guild after a harsh winter storm reduced the amount of available food and altered microhabitats. Stouder (1987) suggested that certain species of surfperch have fixed traits, thereby allowing only those whose morphology is best adapted to harvest available food sources, despite the alteration in their preferred microhabitat. In her study, she suggested that Embiotoca jacksoni and Hypsurus caryi were food limited because winnowing constrains them to foraging in superficial turf that was reduced substantially by the storm. Those that had other means of acquiring prey, picking caprellid amphipods from the reef crest (E. lateralis), or utilizing crabs found in crevices (D. vacca and R. toxotes) were not as affected by the overall lower prey abundance.
The results of the current conclude that behavioral differences (winnowing and nonwinnowing) observed by other studies are not supported by the feeding morphology of surfperches. In other words, there is not a direct link between structure and function for this feeding behavior. Direct measurements have been made in other studies comparing feeding morphology to behavior or performance in other fish groups (Gatz, 1979; Motta, 1988; Wainwright, 1988; Wainwright & Barton, 1995).
However, within the surfperches, it is difficult to show that morphology relates directly to behavior. Given that Embiotoca jacksoni, Hypsurus caryi, and Rhacochilus toxotes are undisputed winnowers according to literature, it was assumed that each species would share similarities in their pharyngeal jaw properties that support this complex processing behavior. Although Hypsurus caryi and Rhacochilus toxotes 18 shared similarities, they both exhibited extreme reduction in their pharyngeal jaw tooth plate and levator posterior / externus 4 musculature that accounts for performance within the pharyngeal jaw (Figure 15). However, Embiotoca jacksoni,
Hypsurus caryi, and Rhacochilus toxotes can be distinguished as species having rather large mouths in comparison to other members of the family (Figures 9, 10 and
11). This suggests that a characteristic of winnowing is possession of a large mouth for biting or scooping up large turf or debris to be processed in their pharyngeal jaws.
Another species, Amphistichus argenteus, also has defining large mouth characteristics. This species is not labeled as a specific foraging type, but this evidence in addition to have moderately advanced pharyngeal jaws (Figure 15) suggests it is likely a winnowing species as well.
In contrast to those species defined as winnowers, Damalichthys vacca
(crusher) exhibited observable difference in morphology. Statistically, D. vacca is unmatched in lower pharyngeal jaw tooth plate mass and in levator posterior/externus
4 mass (Figure 15). Upon dissections of each individual in this project, the D. vacca was the only species with a noticeable difference in size and shape of the lower pharyngeal jaw and associated musculature. This morphological advancement is also supported in literature, meaning that D. vacca is likely to be the only surfperch to utilize large hard-shelled prey (DeMartini, 1969; Ellison, et al., 1979; Haldorson &
Moser, 1979; Laur & Ebeling, 1983). However, data from this experiment also shows that Zalembius rosaceus possess large variations (second only to D. vacca) of both the lower pharyngeal jaw tooth plate and levator muscles. Given its offshore nature 19 and tendency to occur in deeper water (Tarp, 1952), feeding morphology recorded here facilitates utilization of smaller hard-shelled invertebrates (diet of Z. rosaceus) that might explain habitat preference for this species.
Feeding morphology is often an indicator (or sometimes predictor) of how prey are acquired based on the notion that morphology is the underlying factor to performance (Wainwright & Barton, 1995). In this same sense, feeding morphology can also be used as an indicator for diet. Hwever, many gut content analyses or diet studies for surfperch indicate an overlap in the composition of prey eaten (Ellison, et al., 1979; Hixon, 1980; Laur & Ebeling, 1983). Therefore, it is more important to connect how feeding morphology relates to foraging behavior in this family.
Motta (1988) compared the functional morphology of the feeding apparatus in butterflyfishes and determined that the functional significance of the feeding apparatus is best understood in terms of their feeding mechanics (how they eat, rather than what they eat) for this group of fishes as well. Embiotoca lateralis is the one surfperch that is denoted as a visual picker (nonwinnowing) which overlaps in range and diet with its congener (Schmitt and Holbrook 1984). In the environment,
Embiotoca lateralis visually select individual amphipods without the use of winnowing. Interestingly, the morphological data set measured here and analyzed using a PCA cannot differentiate this type of foraging behavior. However, analysis of individual morphometrics does provide some support that explains foraging behaviors both in this species and others. Embiotoca lateralis has very small pharyngeal jaw tooth plates and musculature (Figure 15). This is representative of a species that 20 would not rely on extreme processing of prey using the pharyngeal jaw. Phanerodon furcatus is another species that possesses very small morphology for its pharyngeal jaws. There is limited knowledge regarding this species’ foraging behavior in the environment, but given its reduced pharyngeal jaw structure and the extreme smallness of vertical gape, adductor mandibulae mass, and sternohyoideus mass P. furcatus is also representative of the nonwinnowing behavior seen in E. lateralis.
Variation in feeding morphology
The overall trophic diversity of surfperches is vast. There is no dispute in literature or in this study that individual species differ from one another in their feeding morphology (Figures 9-13, 15, 17). However, data here do not support the notion that each species has features that are reflective of a distinct diet (or specialization), with the exception of the Damalichthys vacca. Rather, surfperch feeding morphology reflects early differentiation among species, thus promoting the potential for resource partitioning and further radiation of this group. It has been suggested that surfperch evolution is a result of resource partitioning and divergence among species into different ecological niches (Bernardi, 2005). Allen, Pondella, &
Horn (2006) classified a few species of surfperches with respect to their broad trophic capabilities: 1) Brachyistius frenatus as a diurnal planktivore; 2) Hyperprosopon argenteum as a large crustacean predator that forages both day and night; 3)
Phanerodon furcatus as a benthivorous carnivore; and 4) those that are able to winnow edible material from mouthfuls of the benthos, such as Embiotoca jacksoni 21 and Rhacochilus toxotes. Perhaps these are examples of ecologically driven resource utilization resulting in trophic specialization within the Embiotocidae.
Highly derived pharyngeal jaw apparatuses are believed to give fish species a successful way of exploiting different prey resources. Mabuchi, Miya, Azuma, &
Nishida (2007) confirmed the importance of pharyngeal jaws and the ability of certain fish clades to diversify based on feeding morphologies. Two main lineages have independently developed highly derived pharyngeal jaws. The first clade includes the
Odacidae, Labridae, and Scaridae and the second the Embiotocidae, Pomacentridae, and Cichlidae. Of the two clades, the Labridae and Cichlidae have received the most attention regarding this trophic novelty. Wainwright et al. (2004) investigated the feeding apparatus of 130 labrid species to explore the morphological and mechanical basis of trophic diversity found in this assemblage. He concluded that the feeding apparatus is morphologically diverse and promotes disparate feeding ecologies among the 130 species. In addition, specific foraging behaviors like planktivores, microcrustacean feeders, molluscivores, and those that feed on large, elusive prey can be distinguished using morphological variables. Prominent foraging behaviors have developed the appropriate morphology that is responsible for such performance.
Within the surfperches, Damalichthys vacca is the only species that really possesses different behaviors and therefore morphology.
Cichlids have achieved evolutionary success that is attributed to the perfection of their adaptations to use different trophic resources within their habitat (Liem,
1973). Many of these adaptations are attributed to their innovative pharyngeal jaw 22 apparatus and trophic specializations. Such specializations include piscivory, insectivory, molluscivory, planktivory, and herbivory. Surfperches seem to be mirroring this concept. However, they have not achieved full niche specialization.
Again, Damalichthys vacca has been the only species to supersede in pharyngeal jaw musculature and dentition by exhibiting extreme hypertrophy that allows them to crush hard-shelled invertebrate prey (molluscivory).
Understanding how species forage in a particular way can sometimes be represented by morphology and how that is associated with specialization and diet.
Most often, feeding morphology can have different behavioral outputs resulting in many ecological benefits, or specialization can constrain the morphology and organism to perform only one task. Liem (1980) found that Petrotilapia tridentiger (a highly specialized rock scraper) was capable of a large range of response and operation, despite its hypothesized limited functionality due to morphological specialization. Surfperch diet does not support the notion of specialization (with the exception of D. vacca). Most diet studies conclude that the majority of items found within the stomachs of surfperch species include isopods, amphipods, gastropods, crabs and shrimp (DeMartini, 1969; Ellison et al., 1979; Laur & Ebeling, 1983;
Ebeling & Laur, 1986). One of the most explainable hypotheses for surfperch being able to achieve successful coexistence is attributed to morphological differences and microhabitat use (Laur & Ebeling, 1983). Although many species of surfperch eat gammerid amphipods, foraging behaviors in different microhabitats (types of substrate and water column depth) would provide the most parsimonious explanation 23 to having significantly different morphology while maintaining successful coexistence.
Behavioral capabilities are determined by morphology which in return, can shape resource use through its effect on performance (Wainwright, 1996). This notion is not supported thus far in what is known about surfperch morphology and behavior.
Several aspects of foraging ecology have been documented (Alevizon, 1975;
Haldorson & Moser, 1979; Hixon, 1980; Schmitt & Coyer, 1982; Schmitt &
Holbrook, 1984; Holbrook & Schmitt, 1986), yet those species that are singled out as having a distinctive way of acquiring prey do not stand out using the morphological variables measured here. Given that there is variation among species of surfperches regarding their feeding morphology, it is possible that they are either still developing specialization (and therefore one day will have morphological traits that explain a certain behavior or foraging tactic) or they have great plasticity in their morphology being able to modify the characteristics they already possess in order to be successful in their current habitat.
Modulation of feeding has been observed in many different groups of fishes.
The feeding apparatus is able to perform a broad spectrum of dissimilar functions within cichlid fishes when faced with differing prey types (Liem, 1980). Within the labrids, Oxycheilinus digrammus was observed to modify kinematic behavior based on live, midwater, and attached prey (Ferry-Graham, Wainwright, Westneat, &
Bellwood, 2001). Furthermore, this notion of attack modulation also has been tested in two species of surfperch, Embiotoca jacksoni and Cymatogaster aggregata. It was 24 shown that E. jacksoni did in fact modulate its strikes on particular prey depending on the necessity of certain mechanics associated with musculature and expansion, whereas C. aggregata was not able to modulate its strike patterns for feeding (Chu,
1989).
Given that the trophic diversity is already high among species of surfperches, potential to even further specialize might still be high. Bernardi & Bucciarelli (1999) concluded that the surfperch family does in fact have a large amount of genetic variation (even compared to that of cichlids), and stated that given these results and the lack of a larval stage, the speciation rate of embiotocids should be high. However, with only 23 species, it remains one of the smaller families of fishes to possess derived feeding morphology. Nonetheless, possession of highly modified pharyngeal jaws lend to the ability to partition resources in shared habitat. Therefore, the surfperch family with high genetic diversity might only be in the beginning stages of specializing morphologies or refining their roles in their respective habitats.
REFERENCES 26
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(Embiotoca lateralis). Copeia, 1975 (4): 608-615.
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California and adjacent waters. University of California Press, Berkeley, CA.
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Bernardi, G. 2005. Phylogeography and demography of sympatric sister surfperch
species, Embiotoca jacksoni and E. lateralis along the California coast:
Historical versus ecological factors. Evolution, 59 (4): 386-394.
Bernardi, G. and Buccuarelli, G. 1999. Molecular phylogeny and speciation of the
surfperches (Embiotocidae, Perciformes). Molecular Phylogenetics and
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Cailliet, G., Love, M., and Ebeling, A. 1986. Fishes: a field and laboratory manual on
their structure, identification, and natural history. Waveland Pr, Inc. Illinois.
Chu, C. 1989. Functional design and prey capture dynamics in an ecologically
generalized surfperch (Embiotocidae). Journal of Zoology; Proceedings of the
Zoological Society of London, 217 (3): 417-440. 27
DeMartini, E. E. 1969. A correlative study of the ecology and comparative feeding
mechanism morphology of the Embiotocidae (surf-fishes) as eveidence of the
family’s adaptive radiation into available ecological niches. The Wasmann
Journal of Biology, 27 (2): 177 – 247.
Ebeling, A. W. and Laur, D. R. 1986. Foraging in surfperches: resource partitioning
or individualistic responses? Environmental Biology of Fishes, 16: 123-133.
Ellison, J. P., Terry, C. and Stephens Jr., J. S. 1979. Food resource utilization among
five species of embiotocids at King Harbor, California, with preliminary
estimates of caloric intake. Marine Biology, 52: 161-169.
Ferry-Graham, L. F., Wainwright, P. C., Westneat, M. W. and Bellwood, D. R. 2001.
Modulation of prey capture kinematics in the cheeklined wrasse Oxycheilinus
digrammus (Teleostei: Labridae). Journal of Experimental Zoology, 290: 88-
100.
Ferry-Graham, L. F., Bolnick, D. I. and Wainwright, P. C. 2002. Using functional
morphology to examine the ecology and evolution of specialization.
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Gatz Jr., J.A. 1979. Community organization in fishes as indicated by morphological
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Haldorson, L. and Moser, M. 1979. Geographic patterns of prey utilization in two
species of surfperch (Embiotocidae). Copeia, 1979 (4): 567-572.
Hixon, M. A. 1980. Competitive interactions between California reef fishes of the
genus Embiotoca. Ecology, 61 (4): 918-931.
Holbrook, S. J. and Schmitt, R. J. 1986. Food acquisition by competing surfperch on
a patchy environmental gradient. Environmental Biology of Fishes, 16: 135-
146.
Horn, M. H. and Ferry-Graham, L. F. 2006. Chapter 14: Feeding mechanisms and
trophic interactions. In: The ecology of marine fishes. Editors Larry Allen,
Daniel Pondella, and Michael Horn. University of California Press, Berkeley,
CA. 1-670.
Laur, D. R. and Ebeling, A. W. 1983. Predator-prey relationships in surfperches.
Environmental Biology of Fishes, 8: 217-229.
29
Liem, K. 1973. Evolutionary strategies and morphological innovations: cichlids
pharyngeal jaws. Systematic Zoology, 22 (4): 425-441.
Liem, K. 1980. Adaptive significance of intra- and interspecific differences in the
feeding repertoires of cichlid fishes. American Zoology, 20: 295-314.
Liem, K. 1986. The pharyngeal jaw apparatus of the Embiotocidae (Teleostei): A
functional and evolutionary perspective. Copeia, 1986 (2): 311-323.
Mabuchi, K., Miya, M., Azuma, Y. and Nishida, M. 2007. Independent evolution of
the specialized pharyngeal jaw apparatus in cichlid and labrid fishes. BMC
Evolutionary Biology, 7 (10): 1-12.
McGowan, C. 1999. A practical guide to vertebrate mechanics. Cambridge:
Cambridge University Press.
Motta, P. J. 1988. Functional morphology of the feeding apparatus of ten species of
Pacific butterflyfishes (Perciformes, Chaetodontidae): an ecomorphological
approach. Environmental Biology of Fishes, 22 (1): 39-67.
Norton, S. F. 1991. Habitat use and community structure in an assemblage of cottid
fishes. Ecology, 72 (6): 2181-2192. 30
Ross, S. T. 1986. Resource partitioning in fish assemblages: a review of field studies.
Copeia, 1986 (2): 352-388.
Schmitt, R. J. and Coyer, J. A. 1982. The foraging ecology of sympatric marine fish
in the genus Embiotoca (Embiotocidae): importance of foraging behavior in
prey size selection. Oecologia, 55: 369-378.
Schmitt, R. J. and Coyer, J. A. 1983. Variation in surfperch diets between allopatry
and sympatry: circumstantial evidence for competition. Oecologia, 58: 402-
410.
Schmitt, R. J. and Holbrook, S. J. 1984. Gape-limitation, foraging tactics and prey
size selectivity of two microcarnivorous species of fish. Oecologia, 63: 6-12.
Stouder, Deanna. 1987. Effects of a severe-weather disturbance on foraging patterns
within a California surfperch guild. Journal of Experimental Biology and
Ecology, 114: 73-84.
Tarp, F. H. 1952. A revision of the family Embiotocidae. Fish Bulletin, 88: 1-99.
Wainwright, P. C. 1988. Morphology and ecology: functional basis of feeding
constraints in Caribbean labrid fishes. Ecology, 69 (3): 635-645. 31
Wainwright, Peter. 1996. Ecological explanation through functional morphology: the
feeding biology of sunfishes. Ecology, 77 (5): 1336-1343.
Wainwright, P. C., and Barton, R.A. 1995. Predicting patterns of prey use from
morphology of fishes. Environmental Biology of Fishes, 44: 97-113.
Wainwright, P. C., Bellwood, D.R., Westneat, M.W., Grubich, J.R., and Hoey, A.S.
2004. A functional morphospace for the skull of labrid fishes: patterns of
diversity in a complex biomechanical system. Biological Journal of the
Linnean Society, 82: 1-25.
Westneat, M. W. 1990. Feeding mechanics of teleost fishes (Labridae; Perciformes):
A test of four-bar linkage models. Journal of morphology, 205: 269-295.
Westneat, M. W. 1995. Feeding, function, and phylogeny: analysis of historical
biomechanics in labrid fishes using comparative methods. Systematic Biology,
44 (3): 361-383.
Westneat, M. W. 2004. Evolution of levers and linkages in the feeding mechanisms
of fishes. Integrative and Comparative Biology, 44: 378-389.
TABLES 33
Table 1. Location and method of collection for surfperch specimens.
# Common Name Scientific Name Collected Collection Location Collection Method Shiner Surfperch Cymatogaster aggregata 16 Elkhorn Slough, Friday Harbor Trawling, Beach Seine Rainbow Surfperch Hypsurus caryi 10 Santa Barbara Scuba Striped Surfperch Embiotoca lateralis 13 Monterey, Friday Harbor Spear Fishing, Beach Seine Black Surfperch Embiotoca jacksoni 10 Santa Barbara Scuba Barred Surfperch Amphistichus argenteus 5 Carmel Bay Unknown Calico Surfperch Amphistichus koelzi 8 Carmel Bay Unknown Rubberlip Surfperch Rhacochilus toxotes 10 Monterey Spear Fishing Pile Surfperch Damalichthys vacca 10 Santa Barbara Scuba, Beach Seine White Surfperch Phanerodon furcatus 8 Santa Barbara Scuba Pink Surfperch Zalembius rosaceus 6 Monterey Bay Trawling
34
Table 2. Principal Components Analysis on 10 morphological variables related to feeding in ten embiotocid species. Table entries are component loadings for each principal axis. Percent variance explained shown in parenthesis. Components that loaded high (> 0.6) are indicated in bold.
Variable PC 1 (26.8%) PC 2 (20.8%) PC 3 (17.8%) PC 4 (12.0%) 1 Jaw Protrusion 0.302 0.289 -0.547 0.370 1 Vertical Gape 0.636 0.178 -0.538 0.180 1 Horizontal Gape 0.439 0.459 -0.389 0.243 1 LoPJ mass 0.524 0.551 0.591 0.052 1 AM mass 0.846 -0.230 -0.040 -0.221 1 SH mass 0.688 -0.508 0.127 -0.335 1 LP mass 0.526 0.516 0.636 -0.029 Maxillary KT -0.271 0.600 -0.275 -0.346 Jaw-Opening MA 0.345 -0.714 0.029 0.431 Jaw-Closing MA -0.240 0.042 0.435 0.707 1 residual from log-log regression with SL
35
Table 3. One way Analysis of Variance (ANOVA) for each PCA explaining 10% or more of the total variance.
Variance Sum of Mean PC Explained Squares df Square F Sig. 1 26.8% 72.118 9 8.013 39.858 < 0.001 2 20.8% 78.962 9 8.774 76.687 < 0.001 3 17.8% 72.679 9 8.075 41.64 < 0.001 4 12.0% 45.806 9 5.09 9.529 < 0.001
FIGURES 37
Figure 1. Head length, standard length and total length measurements made, follows Cailliet et al. 1986.
Head Length (HDL) Standard Length (SL)
Total Length (TL)
38
Figure 2. Diagram showing depression of the lower jaw resulting in protrusion of the upper jaws. Distance measured is indicated by the arrow (see text for details on actual measuring points).
Jaw Protrusion
39
Figure 3. Illustration of vertical and horizontal gape measurement (indicated by arrows).
Vertical Gape
Horizontal Gape
40
Figure 4. Placement of the adductor mandibular (A) and sternohyoideus (B). Actual origins and insertions are detailed in text. Each muscle was removed and weighed. Pictures from Cailliet et al. (1986).
A Lateral View
Adductor Mandibulae I-III
B Ventral View
Sternohyoideus
41
Figure 5. Placement of the levator posterior / externus 4 muscle and lower pharyngeal jaw plate in embiotocids. Both were removed and weighed. Illustration by Ryan Jonna (Animal Diversity Web).
Levator posterior and Levator Externus 4 Muscle
Eye Socket
Premaxilla Upper pharyngeal tooth plate
Lower pharyngeal tooth plate
42
Figure 6. Lower jaw levers for calculating mechanical advantage (Westneat, 1990). See text for descriptions of attachments.
Adductor mandibulae insertion
Quadrate-Articular Joint
Tip of the mandible
Interoperculomandibular ligament
43
Figure 7. Measurements of the four links (open circles) used in calculating the kinematic transmission coefficient, from Westneat (2004). Abbreviations: F, fixed link; N, nasal or coupler link; M, maxillary or output link; J, jaw or input link; D, diagonal.
N Eye
D M F
J
44
Figure 8. Separation of embiotocid species along PC 1 (26.8 %). Species that do not differ significantly (Fisher’s LSD > 0.05) are grouped with a dotted line. A: significance for PC1, B: significance for PC2. Fish illustrations from Allen et al. (2006).
A
Large Vertical Gape Small Vertical Gape Large Adductor Mandibulae Mass Small Adductor Mandibulae Mass Large Sternohyoideus Mass Small Sternohyoideus Mass
45
Figure 8 continued. Separation of embiotocid species along PC 2 (20.8%). Species that do not differ significantly (Fisher’s LSD > 0.05) are grouped with a dotted line. Fish illustrations from Allen et al. (2006).
B
High Maxillary KT Low Maxillary KT
Low Jaw-Opening High Jaw-Opening Mechanical Advantage Mechanical Advantage
46
Figure 9. Boxplot showing differences in adductor mandibulae mass between species. This variable loaded highest on PC 1, characterizing the size of the mouth. Means that are not statistically different from each other (P > 0.05) are underlined.
47
Figure 10. Boxplot showing differences in vertical gape between species. This variable loaded high on PC 1, characterizing the size of the mouth. Means that are not statistically different from each other (P > 0.05) are underlined.
48
Figure 11. Boxplot showing differences in sternohyoideus muscle mass between species. This is the last variable that loaded highest on PC 1. Means that are not statistically different from each other (P > 0.05) are underlined.
49
Figure 12. Boxplot showing differences in jaw opening mechanical advantage between species. This is the first variable to load highest on PC 2, characterizing how fast or forceful the mouth opens. Means that are not statistically different from each other (P > 0.05) are underlined.
50
Figure 13. Boxplot showing differences in the kinematic transmission coefficient (KT) for the oral four-bar linkage mechanism. This is the second variable to load highest on PC 2. Means that are not statistically different from each other (P > 0.05) are underlined.
51
Figure 14. Separation of embiotocid species along PC 3 (17.8 %). Species that do not differ significantly (Fisher’s LSD > 0.05) are grouped with a dotted line. Fish illustrations from Allen et al. (2006).
Large Levator Posterior Muscle Small Levator Posterior Muscle Large Lower Pharyngeal Tooth Plate Small Lower Pharyngeal Tooth Plate
52
Figure 15. Boxplot showing differences of the variable, levator posterior muscle (A), which loaded highest on principle component 3 (17.8%) and the lower pharyngeal jaw mass (B) that loaded next highest. Means that are not statistically different from each other (P > 0.05) are underlined.
A
B
53
Figure 16. Separation of embiotocid species along PC 4 (12.0 %). Species that do not differ significantly (Fisher’s LSD > 0.05) are grouped with a dotted line. Fish illustrations from Allen et al. (2006).
High Jaw Closing Low Jaw Closing Mechanical Advantage Mechanical Advantage
54
Figure 17. Box plot showing differences in jaw-closing mechanical advantage between species. The only variable to load high on PC 4. Means that are not statistically different from each other (P > 0.05) are underlined.
APPENDIX 56
APPENDIX
Morphological characteristics of the body and feeding apparatus in 10 species of embiotocids. Values represent the mean for the sample size given (n) and only adult specimens were used. Please see text for explanations of variables.
Levator posterior Lower Adductor Sterno- / externus Standard Jaw Vertical Horizontal pharyngeal mandibulae hyoideus 4 length protrusion gape gape jaw mass mass mass mass Genus and Species (cm) (mm) (mm) (mm) (g) (g) (g) (g) Amphistichus argenteus (5) 19.1 7.4 26.1 14.5 0.3222 0.6520 1.0763 0.3122 Amphuistichus koelzi (8) 22.7 7.3 18.9 14.1 0.4286 0.7100 1.6246 0.3895 Cymatogaster aggregata (16) 8.9 3.7 9.3 4.9 0.0124 0.0148 0.0601 0.0054 Hypsurus caryi (10) 16.0 5.2 15.0 7.7 0.0715 0.1578 0.7058 0.0522 Embiotoca lateralis (13) 24.7 7.9 21.2 12.4 0.3718 0.7868 2.7724 0.3189 Embiotoca jacksoni (10) 19.1 7.4 19.8 10.7 0.2113 0.5992 1.9371 0.1501 Zalembius rosaceus (6) 9.9 4.3 9.3 5.2 0.0303 0.0308 0.1267 0.0243 Rhacochilus toxotes (10) 33.4 14.5 34.5 19.9 0.9611 2.3499 7.1515 0.9002 Damalichthys vacca (10) 19.4 7.2 18.9 10.4 1.0429 0.3404 1.1685 1.4048 Phanerodon furcatus (8) 14.6 5.1 12.4 7.0 0.0839 0.0706 0.3058 0.0475
57
APPENDIX CONTINUED
Mechanical characteristics of the body and feeding apparatus in 10 species of embiotocids. Values represent the mean for the sample size given (n) and only adult specimens were used. Please see text for explanations of variables. .
Jaw- Jaw- opening closing Maxillary lever lever Genus and Species KT ratio ratio Amphistichus argenteus (5) 0.628 0.172 0.206 Amphuistichus koelzi (8) 0.801 0.161 0.247 Cymatogaster aggregata (16) 0.893 0.122 0.160 Hypsurus caryi (10) 0.690 0.208 0.206 Embiotoca lateralis (13) 0.607 0.239 0.206 Embiotoca jacksoni (10) 0.573 0.266 0.170 Zalembius rosaceus (6) 0.772 0.186 0.171 Rhacochilus toxotes (10) 0.872 0.218 0.227 Damalichthys vacca (10) 0.758 0.174 0.212 Phanerodon furcatus (8) 0.739 0.158 0.207
CHAPTER TWO
FEEDING KINEMATICS IN THE GENUS EMBIOTOCA: MORPHOLOCIAL
COMPARISIONS AND ECOLOGICAL IMPLICATIONS
58
ABSTRACT
Within the surfperch family, two particular congeneric species are noted in literature
as definite winnowers (Embiotoca jacksoni) and pickers (E. lateralis) as well as
competitors that coexist due to behavioral habitat shifts. Feeding kinematics relating
to the oral jaw is described in this study to determine whether or not this supports
documented foraging behavior exhibited in both species. It has been shown (Chapter
1) that these two species differ significantly in their jaw morphology, with the exception of oral jaw mechanics. Both species have very similar values for kinematic transmission coefficient (KT) and jaw closing mechanical advantage. Therefore, kinematic profiles of the oral jaws should reflect these similarities. High speed video was used to capture successful strikes on frozen (dead) krill that was placed into the tank and in camera view. Multiple trials with different individuals of similar sizes were recorded for each species. Video frames were digitized and analyzed using
Image J software. Time to peak maxima and overall average peak maxima of each of the variables was recorded for a total of 10 variables. Of the 10 variables compared in this study, E. jacksoni and E. lateralis only differed significantly in maximum rotation of the maxilla, and in maximum protrusion of the premaxilla. Therefore, data here do not support a distinction between oral jaw kinematics and foraging behavior
(winnowers and pickers). However, since winnowing is a process achieved entirely by the pharyngeal jaws, the ability to capture prey should also be indicative of those behaviors because of how the prey are taken in the natural environment. However, as 59
seen here, E. jacksoni does not use a different capture behavior than that of E. lateralis (when feeding on this particular prey item), suggesting that each species might be able to modulate their behavior based on the type of prey encountered.
60
61
INTRODUCTION
Using functional morphology of fish feeding mechanisms can be a powerful tool when applications of ecological issues are being considered (Wainwright &
Bellwood, 2002). This notion of how morphology might influence ecology is not a novel idea, and has been ongoing for decades. Its application here, comparing the kinematics in the two congeners Embiotoca lateralis and Embiotoca jacksoni, provides an opportunity to investigate the ecology of these two closely related species that give live birth and possess highly derived pharyngeal jaws. They exhibit an almost parallel existence in 1) their body and feeding morphology; 2) habitats and ranges; and 3) diet composition. Both E. lateralis and E. jacksoni all come from a group of fishes with a generally deep, elliptical, laterally compressed body
(DeMartini, 1969). They all possess a highly developed pharyngeal jaw apparatus
(Liem, 1986) and give birth to extraordinarily well-developed live young (Tarp,
1952), meaning that they do not disperse far and therefore live and forage within small, tightly overlapping ranges (Bernardi, 2005)
In a study conducted by Motta (1988) using 10 species of butterflyfishes, there were considerable differences in morphology among these species. However, many retained plasticity in their prey choice despite these differences. Therefore, guild identity was assigned based upon how prey were captured as opposed to diet composition, revealing that similarity in diets did not necessarily correspond to similarity in morphology. This particular study is of importance because eight of the
10 species sampled were in the same genus, and the remaining two were within a 62 second genus. Despite the close relationships of these particular fishes, drastic differences were observed in their morphology, thereby permitting them to feed on similar items but in different ways.
Embiotoca lateralis and E. jacksoni overlap greatly in their geographic ranges and as a result utilize similar prey resources. However, there has been an observable difference in their ability to acquire prey. Embiotoca lateralis usually favors a non- winnowing approach (picking) versus E. jacksoni that winnows extensively. Both these species acquire prey (in their oral jaws) by use of suction; however, winnowing a large mass of material versus just one item is a task that is processed using the pharyngeal jaws. Many studies have compared these two species with regard to their spatial overlap and potential competition for food resources by analyzing gut contents and observational data in the field. Some of the major findings according to researchers are that diets are consistently similar, comprised mostly of gammarid amphipods (Schmitt & Coyer, 1982, 1983; Holbrook & Schmitt, 1986).
Foraging modes might account for a separation between E. lateralis and E. jacksoni in habitat use based on depth and substrate. Hixon (1980), through experimental evidence, showed that even though both species exhibit similar diets, prey is acquired at deeper depths over turf substrate for E. jacksoni and in shallower waters over fleshy red alga for E. lateralis. In addition, the types of gammarid amphipods utilized differed between those that are “free-living” for E. lateralis and
“tubicolus” for E. jacksoni (Schmitt & Coyer, 1982; 1983). This evidence supports 63 the ability then of Embiotoca jacksoni to winnow different material within the same habitat as E. lateralis, potentially demonstrating the partitioning of resources.
Morphological data presented in Chapter 1 showed significant differences in jaw protrusion, vertical gape, horizontal gape, mass of the lower pharyngeal jaw, mass of the adductor mandibulae, mass of the sternohyoideus, mass of the levator posterior muscle, closing mechanical advantage, and opening mechanical advantage between Embiotoca lateralis and Embiotoca jacksoni. Oddly, only one remaining variable that was measured showed no significant difference between E. lateralis and
E. jacksoni, the kinematic transmission coefficient (KT) which is a quantification used and tested in some groups of fishes to represent prey capture abilities dealing with the oral jaws. This suggests there may be some similarity in the way the jaws move, despite the differences observed in the underlying morphology.
There are many possibilities or ways to modulate morphology to potentially produce more than one outcome (Wagner & Altenberg, 1996). Norton (1991) showed that species in the fish family Cottidae had the ability to modify their attack kinematics depending on the type of prey and the escape tactic it employed. Further, differences in feeding kinematics can be associated with different microhabitats.
Ferry-Graham, Wainwright, Westneat, & Bellwood (2002) showed that among five different species of labrids, kinematic profiles differed for each species between prey attached to the benthos versus prey suspended midwater. Therefore, the underlying morphology within each labrid species has the ability to modulate its behavior depending on the prey type it encounters. This ability, in which morphology can 64 produce multiple outcomes, is a concept called “many-to-one-mapping” (Collar &
Wainwright, 2006). These authors showed, in a group of centrarchid fishes, that multiple alternate forms in morphology can produce the same mechanical properties
(in this case, magnitude of suction generated for feeding strikes). Since species within the genus Embiotoca possess different jaw morphology, they might share similar kinematics when foraging on the same prey resources.
Data collected here will help answer or support which factors are currently governing the behaviors observed in literature to explain how E. jacksoni and E. lateralis are able to live in close proximity without serious competition. Therefore, if
Embiotoca lateralis and E. jacksoni feed using instinctive behaviors (winnowing versus picking), results should indicate they use kinematics more consistent with their foraging choice. To corroborate this story, the kinematics during multiple strike sequences for both species were analyzed using high-speed video. The winnower
Embiotoca jacksoni should produce different strike kinematics than the picker E. lateralis.
METHODS
Specimens of Embiotoca jacksoni (HL: 32 mm, 35 mm, 41 mm,) were collected by otter trawl in Elkhorn Slough, Calif. Embiotoca lateralis (HL: 31 mm, 33 mm, 36 mm) were captured by net using SCUBA in Stillwater Cove in Pebble Beach,
Calif. Upon capture, both species were brought to the lab and allowed to acclimate in individual 20-gallon running seawater aquaria for a minimum of 2 weeks. Collection was conducted under the permission of the California Department of Fish and Game 65
(permit # 816403) and in accordance with San Jose State University IACUC protocol
814. All fish were provided with a consistent diet of small frozen krill, which was also the test prey item. Both species fed readily on this item and would strike at individual krill (0.5 – 1.0 cm) in the water column.
All three individuals of each species provided data for kinematic analysis.
Events were captured with a Redlake Imaging MotionScope® model PCI 2000 S filming at 250 frames per second. Two Smith-Victor Corp bi-pin tungsten halogen flood lamps, model 700 SG, were also used to illuminate the subjects. Filming occurred with a black backdrop and attached scale for reference while individual fish swam continuously around the tank. Multiple feeding events were captured; however, only three successful strikes were selected for further analysis per individual. A successful strike was chosen based on the lateral position of the fish in the image and the visibility of the landmarks used for measurement (Figure 1). Feeding events start at the frame just prior to mouth opening (t0) and end at the frame after the mouth has
closed.
Every other frame was digitized in each film sequence using Image J by NIH
(http://rsb.info.nih.gov/ij/index.html). Selected kinematic variables were measured following Westneat (1990) (Table 1). Correction of the data to head length (HL) did not differ from uncorrected data, so actual values were used. These measurements were graphed and mean peak maxima and time to peak maxima were calculated for each variable for each individual. These maxima were compared between E. jacksoni 66 and E. lateralis using a two-sample t-test with a sequential Bonferroni correction test
(Rice 1988).
RESULTS
The strike behaviors of both species were quite similar. Each strike was initiated with the onset of the mouth opening (Figure 2B). It can be clearly observed in the sequences shown that Embiotoca lateralis initiated mouth opening further from the prey item (Figure 2B, E. lateralis) than E. jacksoni. The peak maxima of all variables measured, coincided with the mean time to peak maximum and the frame at which prey entered the mouth (Tables 2, 3; Figure 2C). Both species approached the prey item, initiated mouth opening, and captured the prey item around the same time.
However, once the prey was captured, Embiotoca jacksoni initiated mouth closing before E. lateralis and right after prey consumption (E. jacksoni: Figures 2D, 2E).
Mouth closing was delayed slightly in E. lateralis (Figure 2E), therefore altering the timing of sequences between species.
The first variable to reach maximum during a prey strike for both species was cranial elevation. Embiotoca jacksoni had a mean cranial elevation of 6.66 degrees and E. lateralis had a mean of 5.31 degrees (Table 2). Although the actual peak maxima and the mean time to peak maxima were not statistically significant (t =
2.967, P = 0.009), timing of cranial elevation happened slightly faster in E. jacksoni
(47.1 ms) than in E. lateralis (51.6 ms) (Tables 3, 4). For E. jacksoni, after the cranium had elevated, the maxilla maximally rotated (52.4 ms), followed by 67
simultaneous peak premaxillary protrusion and gape expansion (54.2 ms), ending with the full extension of the lower jaw at 56.9 ms (Table 3; Figure 3).
However, for E. lateralis these last four movements associated with mouth opening occurred simultaneously all at 56.9 ms (Table 3; Figure 3).
Significant differences were detected between E. jacksoni and E. lateralis in maxillary rotation and premaxillary protrusion. Embiotoca jacksoni achieved a significantly smaller angle of maxillary rotation (35.07 vs. 41.64 degrees) than E. lateralis (Table 2, 4). Therefore, E. lateralis rotated its maxilla more. However, this was in the about the same length of time as E. jacksoni (Figure 3). Since their maximum gape is similar (Table 2), E. lateralis necessarily used a larger rotation of the maxilla to achieve maximum gape. The difference in premaxillary protrusion between E. jacksoni and E. lateralis was small (0.58 cm vs. 0.44 cm), but significant
(Table 4). Therefore, E. jacksoni rotated its maxilla less but achieved a greater premaxilla protrusion distance. Again, there was no difference in the time to the peak maximum of this variable between the two species (Table 3, 4; Figure 3). The last two kinematic variables measured, gape distance and lower jaw depression were not significantly different between the two species (Table 2, 4); nor did the time to reach these maxima differ significantly (Table 3, 4).
DISCUSSION
Both species exhibited very similar prey capture behaviors, despite having different oral jaw morphology. The kinematics in this study showed almost identical trends between the two congeneric species studied. Thus, the classification of 68 winnower versus picker cannot be distinguished among the variables listed here, which is quite surprising given the morphological data collected from Chapter 1. Of the eight variables measured relating to oral jaw feeding, Embiotoca lateralis and E. jacksoni only share one that is not statistically significant, the oral four-bar linkage kinematic transmission coefficient (KT). This variable is a ratio of the amount of output motion sustained or initiated by a certain input motion relating to a series of links aligned in a plane. These particular links associated with the KT value are direct measurements of the oral jaws (just like the ones calculated from high-speed video analysis). The fact that these series of connected links governing movement of the oral jaws are similar in both species, lends to explaining why they produced almost identical prey capture kinematics.
Maxillary rotation and premaxillary protrusion distance were the two variables that differed statistically between E. jacksoni and E. lateralis. Maxillary rotation is one of three predicted movements from calculations resulting from the oral four-bar linkage (Westneat, 1990). This is the one variable that both E. jacksoni and
E. lateralis had similar values for in Chapter 1. It is interesting then, that of the kinematics measured here, they would produce statistically different results.
Embiotoca lateralis had a maximum rotation angle of 41.6 degrees compared to 35.1 degrees in Embiotoca jacksoni. Furthermore, this maximum is achieved by depression of the lower jaw which was identical for each species. Principles for four-bar linkages demand that maxillary rotation be coupled with lower jaw depression because the two elements are members of the same four-bar chain (Westneat, 1990). In addition, 69 premaxillary protrusion distance was greater in Embiotoca jacksoni (0.58 cm) than in
E. lateralis (0.44 cm) which was not expected given that E. lateralis produces a much larger maxillary rotation. Therefore, it seems as though E. lateralis is generating less efficient oral jaw kinematics than E. jacksoni.
The oral jaw kinematics recorded in this study can be used to interpret ecological interactions among Embiotoca lateralis and E. jacksoni. However, some of the kinematic data collected here do not seem consistent with the way each species forages. Embiotoca lateralis relies on its ability to pick individual prey out of the water column. Utilizing this type for foraging behavior would benefit from having an extensive premaxillary protrusion, small gape and rapid depression of the lower jaw in order to facilitate suction (Horn & Ferry-Graham, 2006). However, E. lateralis has reduced premaxillary protrusion achieved by a higher rotation of the maxilla that results in the same gape distance as E. jacksoni. Therefore, suction potential would be less in species of E. lateralis than in E. jacksoni. Laur and Ebeling (1983), state that
E. lateralis is defined as a generalist because it neither has the ability to crush hard- shelled prey or winnow inedible material from edible material, thus limiting its foraging efficiency.
There have been observations of aggressive behavior exhibited by E. lateralis toward other members of the family chasing them from profitable feeding areas
(Hixon, 1980). This aggression might be linked to the inability of E. lateralis to forage efficiently. However, as a result of their foraging ability during periods when these two species overlap in habitat, E. lateralis will maintain a position in shallower 70 water while “excluding” E. jacksoni to deeper water (Hixon, 1980). The resources that both of these fishes prey upon include such things as polychaetes, ophiuroids, and other shrimp species, with the majority of the diet encompassing gammarid and caprellid amphipods (Ellison, Terry, & Stephens, 1979; Haldorson & Moser, 1979;
Laur & Ebeling, 1983; Ebeling & Laur, 1986; Holbrook & Schmitt, 1986). It has been observed through these studies that abundance and diversity of crustacean prey decreases with depth where these two species occur (Schmitt & Holbrook, 1986).
Therefore, the optimal foraging area is located in shallower depths (reef crest), while less productive foraging areas are at greater depths (reef slopes). If its foraging efficiency is reduced, it would benefit E. lateralis to maintain position where the most profitable prey items are found. In fact, E. lateralis spends a great amount of time searching for large, high-calorie prey items that might occur less frequently (Schmitt
& Coyer, 1982).
Many studies have concluded that foraging behavior is most important when describing the diet of these two species (Alevizon, 1975; Laur & Ebeling, 1983;
Schmitt & Holbrook, 1984). However, they fail to provide numerical data to support the morphology behind such behavior. The kinematics of prey capture provided here detail the behavioral responses in both E. lateralis and E. jacksoni and were able to show similarities within the oral jaw movement of two congeneric species despite their different foraging behaviors and overall morphology. Embiotoca jacksoni has morphology that is able to capture and handle prey in much the same way as E. lateralis or is able to modulate its behavior without having to sacrifice its 71 specialization to winnow. Chu (1989), described the ability for Embiotoca jacksoni to modify its attack depending on type of prey presented and Embiotoca lateralis was able to modulate their pressure generation based on changes in prey type (Drucker &
Jensen, 1991). The trophic capabilities of surfperch have led to many studies given their unique situation; a situation that brings many species within the same family to inhabit or occupy the same areas. They have accomplished this with remarkable ability to exist in this dynamic environment together by incorporating key identifying performance differences that allow members of this family to exploit resources that another cannot.
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TABLES 82
Table 1. Measurements made to produce kinematic variables (Westneat, 1990). Vertex for each angular measurement is listed second (i.e. angle ABC, B is the vertex). Letters represent landmarks in Figure 1.
Variable Measurement Landmarks Cranial Elevation Angle between the dorsal tip of the rostrum to the Figure 1: CHK cranium between the eye and first dorsal spine origin (vertex) to the origin of first pectoral fin ray
Maxillary Rotation Angle between the maxilla-premaxilla junction to the Figure 1: DCH dorsal tip of the rostrum (vertex) to the cranium between the eye and first dorsal spine origin
Lower Jaw Depression Angle between the origin of the first pectoral fin ray to Figure 1: KEB the mandible/quadrate articulation (vertex) to the tip of the dentary
Premaxillary Protrusion Distance between the posterior-most point of the eye Figure 1: GA orbit to anterior tip of premaxilla
Gape Distance Distance between the anterior premaxilla tip to the Figure 1: AB anterior tip of the dentary
83
Table 2. Mean peak maxima and standard error for all five kinematic variables measured during high speed video. Measurements in degrees (o) and in centimeters (cm).
Peak Maximums
Embiotoca jacksoni Embiotoca lateralis
Kinematic Variables MEAN SE MEAN SE
Cranial Elevation (o) 6.7 2.0 5.3 0.2
Maxillary Rotation (o) 35.1 1.8 41.6 0.5
Premaxillary Protrusion (cm) 0.6 0.0 0.4 0.0
Gape Distance (cm) 0.7 0.0 0.6 0.0
Lower Jaw Depression (o) 32.1 2.0 33.7 0.8
84
Table 3. Mean time to peak maxima and standard error for all five kinematic variables measured during high speed video. Measurements in milliseconds (ms).
Time to Peak Maximums
Embiotoca jacksoni Embiotoca lateralis
Kinematic Variables MEAN SE MEAN SE
Cranial Elevation (ms) 47.1 2.5 51.6 3.8
Maxillary Rotation (ms) 52.4 3.3 56.9 3.4
Premaxillary Protrusion (ms) 54.2 4.2 56.9 3.6
Gape Distance (ms) 54.2 1.8 56.9 2.8
Lower Jaw Depression (ms) 56.9 3.6 56.9 3.1
85
Table 4. Results of t values for differences among Embiotoca jacksoni and Embiotoca lateralis for each kinematic variable. Significance is determined by a sequential Bonferroni correction test (Rice, 1989) using an initial ά of 0.05. The degrees of freedom for each test are 16. Significance is noted below. Kinematic Variables Bonnferroni Peak Maximums t P table-wide correction Significant
Cranial Elevation (o) 2.967 0.009 0.006 No
Maxillary Rotation (o) -3.484 0.003 0.006 Yes
Premaxillary Protrusion (cm) 4.278 0.001 0.005 Yes Gape Distance (cm) 0.958 0.352 n/a No Lower Jaw Depression (o) -0.769 0.453 n/a No
Time to Peak Maximums
Cranial Elevation (ms) -0.981 0.341 n/a No Maxillary Rotation (ms) -0.941 0.361 n/a No Premaxillary Protrusion (ms) -0.482 0.636 n/a No Gape Distance (ms) -0.802 0.434 n/a No Lower Jaw Depression (ms) 0 1.0 n/a No
FIGURES 87
H C A G
B D E K
Figure 1. Landmarks associated with measurements made for all kinematic variables from Westneat, 1990: A) anterior premaxilla tip; B) anterior dentary tip; C) dorsal tip of rostrum (dorsal-most visible point of maxilla); D) maxilla-premaxilla junction; E) mandible/quadrate articulation; G) posterior-most point of orbit of eye; H) cranium between eye and first dorsal spine origin; and K) origin of first pectoral fin ray.
88
Embiotoca jacksoni
A B C D E
Embiotoca lateralis
A B C * D
t = 0 t= 16 t = 48 t = 72 t = 96
Figure 2. Still frames from high speed video showing prey capture and expression of kinematic variables through time. Arrow indicates prey item. The frames represent A) beginning of sequence B) onset of mouth opening C) peak maxima and moment of capture D) start of mouth closing *) mouth held open through prey capture and E) mouth closed. Approximate time (t) is shown for these individuals in milliseconds (ms). 88
89
♦ Embiotoca jacksoni ■ Embiotoca lateralis
Figure 3. Strike patterns (angles) for Embiotoca jacksoni (♦) and Embiotoca lateralis (■).The mean was taken from three feeding events each from three individuals per species and the bars indicate standard error. 90
♦ Embiotoca jacksoni ■ Embiotoca lateralis
Figure 3 continued. Strike patterns (distance) for Embiotoca jacksoni (♦) and Embiotoca lateralis (■).The mean was taken from three feeding events each from three individuals per species and the bars indicate standard error. 90