Eat whole and less often: ontogenetic shift reveals size specialization on kelp bass by the California moray eel, Gymnothorax mordax

Abstract

Despite the importance of predation in many ecosystems, gaps remain in our understanding of nocturnal marine predators. Although the kelp forests of Southern California are some of the most well-studied ecosystems, California morays, Gymnothorax mordax, are predominately nocturnal predators that have remained largely unstudied and their predatory effects on the kelp forest ecosystem are unknown. We use a multi-year data set to examine the dietary breadth of G. mordax and to determine the functional role of this predator. We also quantify bite force to examine the potential performance limitations of morays in exploiting prey. Stomach content analyses and linear selectivity index values indicate that G. mordax specializes on kelp bass, Paralabrax clathratus. Average size of kelp bass consumed varies across years, suggesting that morays respond to fluctuations in prey size availability. The scaling relationship of kelp bass standard length and moray head length reveals an ontogenetic shift, where maximum prey size increases with moray size and small prey are dropped from the diet of larger individuals. Moray bite force exhibited strong positive allometry with moray head size, suggesting that larger morays exhibit greater bite forces for their head and body size. However, we found no relationship between prey size and bite force, suggesting that a disproportional increase in bite force does not facilitate the consumption of disproportionately larger prey. Our results indicate that while G. mordax of Catalina Island is a dietary specialist, it is capable of exhibiting functional shifts in prey size and species based on their abundance.

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Oecologia (2018) 188:875–887
https://doi.org/10.1007/s00442-018-4260-x
COMMUNITY ECOLOGY – ORIGINAL RESEARCH
Eat whole andlessoften: ontogenetic shift reveals size specialization
onkelp bass bytheCalifornia moray eel, Gymnothorax mordax
BenjaminA.Higgins1 · ChrisJ.Law1· RitaS.Mehta1
Received: 24 March 2018 / Accepted: 8 September 2018 / Published online: 18 September 2018
© The Author(s) 2018
Abstract
Despite the importance of predation in many ecosystems, gaps remain in our understanding of nocturnal marine predators.
Although the kelp forests of Southern California are some of the most well-studied ecosystems, California morays, Gym-
nothorax mordax, are predominately nocturnal predators that have remained largely unstudied and their predatory effects
on the kelp forest ecosystem are unknown. We use a multi-year data set to examine the dietary breadth of G. mordax and to
determine the functional role of this predator. We also quantify bite force to examine the potential performance limitations
of morays in exploiting prey. Stomach content analyses and linear selectivity index values indicate that G. mordax special-
izes on kelp bass, Paralabrax clathratus. Average size of kelp bass consumed varies across years, suggesting that morays
respond to fluctuations in prey size availability. The scaling relationship of kelp bass standard length and moray head length
reveals an ontogenetic shift, where maximum prey size increases with moray size and small prey are dropped from the diet of
larger individuals. Moray bite force exhibited strong positive allometry with moray head size, suggesting that larger morays
exhibit greater bite forces for their head and body size. However, we found no relationship between prey size and bite force,
suggesting that a disproportional increase in bite force does not facilitate the consumption of disproportionately larger prey.
Our results indicate that while G. mordax of Catalina Island is a dietary specialist, it is capable of exhibiting functional shifts
in prey size and species based on their abundance.
Keywords Dietary specialization· Kelp bass· Morays· Bite force· Predator–prey size relationships
Introduction
Predation dramatically affects the dynamics, relative abun-
dance, and distribution of prey populations thereby influ-
encing the pattern and direction of energy flow from lower
to higher levels in food webs (Morin 2011). The effects
predators have on their prey depends on the degree of prey
specialization which is often dictated by a predator’s mor-
phology (Werner 1977; Persson etal. 1996; Wainwright and
Richard 1995) and whether predators themselves respond
to changes in prey availability and density (Redpath and
Thirgood 1999). Classification of predators as specialists
or generalists informs the functional role of predators and
how they may respond to fluxes in prey density (Anders-
son and Erlinge 1977). Whereas specialists tend to respond
to changes in prey densities by immigrating to a new prey
patch, generalists can respond similar to specialists or can
respond functionally via prey switching (Murdoch 1969;
Andersson and Erlinge 1977; Redpath and Thirgood 1999).
Such frequency-dependent predation has shown to have
a stabilizing influence on prey numbers (Redpath and
Thirgood 1999) and maintain overall biodiversity in the
ecosystem.
The terms ‘specialist ‘and ‘generalist’ also describe the
breadth of the dietary niche. However, dietary niche is not
only defined by the types of prey consumed but also by
prey size. Prey size is particularly important when inves-
tigating how feeding behavior and diet may change over a
species’ lifetime. There are a myriad of reasons as to why
Communicated by Donovan P. German.
Electronic supplementary material The online version of this
article (https ://doi.org/10.1007/s0044 2-018-4260-x) contains
supplementary material, which is available to authorized users.
* Benjamin A. Higgins
bahiggin@ucsc.edu
1 Department ofEcology andEvolutionary Biology, Center
forCoastal Biology, 130 McAllister Way, SantaCruz,
CA95060, USA
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876 Oecologia (2018) 188:875–887
1 3
predators may become more successful at capturing prey
at larger body sizes (i.e., increased muscle mass, larger
gape, increased endurance). Therefore, it is expected that
changes in body size may result in a linear shift in prey
size (Arnold 1983; Persson 1990; Juanes 1994; Mittel-
bach and Persson 1998; Jacobson etal. 2018). Scharf etal.
(2000) discovered that while larger predators (> 500mm)
tend to exhibit a narrowing in the breadth of relative prey
sizes consumed over ontogeny (i.e., ontogenetic shift),
asymmetric predator–prey size distributions appear to be
a common pattern in aquatic communities (ontogenetic
telescoping). These two patterns, ontogenetic shift and
ontogenetic telescoping, which differ by whether small
prey are dropped or maintained in the diet of large individ-
uals, are important factors in determining predator–prey
dynamics (Shurin etal. 2006) and provide a framework
for understanding the mechanisms of the observed preda-
tor–prey relationships (Woodward etal. 2005; de Roos
and Persson 2013).
Studying the ontogenetic changes to the underlying
functional morphology of the feeding apparatus can also
contribute insight into understanding predator–prey relation-
ships. Functional measures of feeding performance such as
bite force have potential to indicate resource use among the
potential prey available (Osenberg and Mittelbach 1989;
Pérez-Barbería and Gordon 1999; Marshall etal. 2012).
Ontogenetic changes in bite force can facilitate specializa-
tion or generalization on different prey types and/or sizes
and can, therefore, be used to elucidate asymmetries in
resource use. For example, individuals that can exert greater
bite forces can expand their dietary breadth by consuming
larger or more robust food items (Verwaijen etal. 2002; Her-
rel etal. 2006; Bulté etal. 2008) and/or reducing handling
times for both prey capture and consumption (Verwaijen
etal. 2002; van der Meij and Bout 2006; Anderson etal.
2008). Thus, the maximum size of prey predators may be
able to consume should change throughout ontogeny (Erick-
son etal. 2003; Sánchez-Hernandez etal. 2012). We expect
that predator–prey size relationships will be especially
strong in piscivorous predators that consume prey whole.
In this study, we examine the dietary ecology of the Cali-
fornia moray eel, Gymnothorax mordax. A previous study
revealed that morays, in general, exhibit specialized mor-
phology for both the capture and transport of large prey
(Mehta and Wainwright 2007). More recently, we have found
that head length and vertical gape distance in the California
moray increase disproportionately over ontogeny (Harrison
etal. 2017), suggesting that the moray-feeding apparatus
may be under strong selection to quickly increase gape size
enabling larger individuals to consume larger prey items
(Mittelbach 1981; Wainwright and Shaw 1999). Neverthe-
less, no study has recorded diet of the California moray in
any detail and examined predator–prey size relationships.
Although researchers have traditionally identified Califor-
nia morays as predators in Southern California kelp forests
with diverse prey handling strategies (Diluzio etal. 2017),
their prey breadth remains unknown. The paucity of dietary
information stems from the fact that California morays were
thought to be relatively rare (Graham 2004; Froeschke etal.
2006). Recent work, however, revealed that the larvae of
these cryptic predators are brought to Catalina Island dur-
ing episodic El Niño events (Higgins etal. 2017) resulting
in an abundant and relatively large biomass (~ 173.83kg) of
G. mordax within the rocky reefs of Two Harbors, Catalina
Island (Higgins and Mehta 2017). As El Niño events have
been shown to greatly alter the distribution of larval fish
and resultant fish assemblages (Cowen 1985; Allen etal.
2002), one would anticipate temporal variation in preda-
tor–prey size relationships. Assessing temporal changes
would require dietary analyses each year and over con-
secutive years, preferably incorporating dynamic climactic
events such as an El Niño.
Here, we used a multi-year data set, incorporating the
2015 El Niño, to examine annual dietary patterns and to
detect any size-based feeding habits of the California moray
eel. Our objectives of this study were threefold. First, we
examined the dietary breadth and determined, where the
California moray fits on a continuum from generalist to
specialist with respect to prey available in the environment.
Second, we recorded invivo bite force for a size range of
morays to examine how feeding performance changes over
ontogeny. Third, we use information on prey size and moray
size to test whether average prey size increased over ontog-
eny. Through this multifaceted approach, we can better
understand the trophic position and functional role of this
elusive but abundant predator inhabiting the southern Cali-
fornia kelp forest ecosystem.
Materials andmethods
Trapping
Gymnothorax mordax were collected using custom-built,
dual-chambered wire mesh traps (N = 20, 36″ × 11″ × 9″;
Staten Island, NY) during the mid-late summer months
(July–September) from 2012 to 2016 around Two Harbors,
Catalina Island, CA (33°26′45.4″N, 118°29′31.3″W). Traps
were set daily between 1800 and 1900h and baited with
frozen anchovies, which were placed into perforated plastic
bottles allowing odor to serve as an attractant while prohibit-
ing access to the bait. Mesh traps were randomly deployed
within six trapping sites spread across four coves in Two
Harbors (Fig.1). Additional traps were set east of Lion’s
Head Point (33°27′10.58″N, 118°30′3.94″W), and the slopes
between Cherry and Fourth of July Coves (33°26′56.74″N,
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877Oecologia (2018) 188:875–887
1 3
118°29′57.49″), as well as Fourth of July and Isthmus coves
(33°26′45.20″N, 118°29′52.44″W). These traps were used
as the start/end points for prey availability and abundance
transects. Traps were deployed around 1600h and retrieved
the following morning between 7:30 and 9:30am.
Gut content analysis andmorphological
measurements
Trapped G. mordax were brought onboard a 6m skiff.
Individuals were placed in a lidded bucket filled with sea-
water and Tricaine Methanesulfonate (MS-222) buffered
with sodium bicarbonate at roughly 90mg/l. Once sedated,
moray mass (g), total length (LT, mm; defined as distance
from anterior tip of snout to posterior tip of tail), head
length (LH, mm; defined as the linear distance between
the anterior tip of the head and the posterior edge of the
parabranchial opening), and head width (Lw, mm defined
as the linear distance spanning the lateral sides of the A2
subdivision of the adductor mandibulae muscles) were all
recorded. Following these morphometric measurements,
morays were examined for gut contents. We obtained
consumed items via manual palpation, an effective and
non-invasive method for recovering recently ingested
items that is commonly used to obtain gut contents from
snakes, another elongate predator that consumes prey
whole (Mushinsky and Hebrard 1977; Fitch 1987). Prey
items within the gut were massaged up from the bottom
of the stomach and into the mouth from where they were
carefully extracted with forceps (Fig.2). All dietary items
recovered were identified to lowest taxonomic group, and
maximum lengths (mm) for whole prey were recorded.
Fig. 1 Map of two harbors, Cat-
alina Island. Trapping locations
are displayed in bold font. Ovals
represent locations, where prey
availability and abundance tran-
sects were conducted in 2013
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878 Oecologia (2018) 188:875–887
1 3
Prey availability andabundance
Observations of potential invertebrate and vertebrate prey
were obtained from Reef Check California’s online Global
Reef Tracker database. These data enabled us to analyze
prey availability and abundance for all years included in the
present study (2012–2016). Reef Check California surveys
the relative abundance and size distribution of species using
a methodology based on the Department of Fish and Game’s
Cooperative Research and Assessment of Nearshore Eco-
systems (CRANE) monitoring program. Transects are con-
ducted in both onshore and inshore reefs with a maximum
depth limit of 18m, with a series of three transects spanning
30m each. Transects are conducted annually at the same
sites in which morays were collected. In 2013, we conducted
our own prey availability and abundance transects to cor-
roborate the Reef Check survey results and found strong
correspondence (see supplemental materials).
To categorize morays as predators on a continuum from
generalist to specialist, we used the linear selectivity index
(L; Strauss 1979), which requires knowledge of both the prey
items available in the environment and those found through
gut content analyses. L selectivity is a unitless number and
is the unweighted difference of the proportions of prey items
found in the gut and the same item(s) recorded in the habitat.
Thus, an L value of 0 would indicate that G. mordax is not
specializing on any particular prey item(s) and is a generalist
consumer, whereas a value closer to 1 suggests that there is
strong specialization for a particular prey, while negative L
values indicate avoidance, or inaccessibility of prey.
Bite force
To quantify moray-feeding performance over ontogeny, we
measured invivo bite force for as many of the trapped indi-
viduals as possible. We used a piezoelectric force transducer
(Kistler Quartz Force Sensor type 9203) mounted between
custom-made steel cantilever beams and fitted with a hand-
held charge amplifier (Kistler type 5995A). Steel bite plates
were fixed onto the cantilever beams and set 2.4cm apart.
Following recommendations from Lappin and Jones (2014),
we covered the steel bite plates with leather to reduce stiff-
ness of the bite plates and to avoid subjecting morays to pos-
sible tooth and jaw damage during biting trials. We recorded
maximum bite forces from trapped individuals. An individ-
ual moray was placed in a 5gallon bucket to constrain the
body of the animal and the force transducer was positioned
in front of the moray’s mouth to elicit biting. All bite force
data were recorded from anterior bites. Therefore, morays
presumably bit with the peripheral and median intermaxil-
lary teeth and teeth along the anterior dentary of the oral
jaws. We then sedated each individual to record the same
suite of morphometric data (mass, total length, head length,
and head width) as described above, and then released indi-
viduals to their original coves, once they recovered from
anesthesia. These data were collected during the 2015 and
2016 summer months.
Statistical analyses
All statistics were carried out in R 3.4.1 (R Core Team
2017). For each year, we tallied the number of prey items
and taxonomically grouped items (e.g., fishes, crustaceans,
and mollusks) found in the moray diet. We tested whether
the number of prey items consumed and whether the pro-
portions of different types of prey items consumed varied
between years using Kolmogrov–Smirnov tests. Repeated
Hotelling’s two-sample t tests were used to determine if
consumed prey proportions differed across years (R pack-
age “Hotelling”). For each year, we also presented the size
distribution of kelp bass prey, because we found kelp bass to
be the dominant prey for morays (see Results). We tested for
differences in the sizes of kelp bass consumed across years
using an ANOVA followed by a Tukey’s honest significant
test (HSD) to examine pairwise differences across years. The
Fig. 2 a Prey bolus indicated by circle on sedated G. mordax. b
Example of how we extract a prey item in this case, kelp bass, using
forceps. The item was first massaged towards the oral jaws via man-
ual palpation
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879Oecologia (2018) 188:875–887
1 3
variances of the annual kelp bass sizes were tested using
Levene’s test for equal variance.
We examined scaling relationships between moray size
and bite force using standardized major axis (SMA) regres-
sions in the R package smatr. Moray size measurements
included the following morphometrics in mm: body mass,
body length, head length, and head width. Scaling relation-
ships were statistically compared using modified t tests with
null predictions of the isometric slopes: 1.0 for linear meas-
urements, 2.0 for areas and forces, and 3.0 for masses based
on Euclidean geometry (Hill 1950; Schmidt-Nielsen 1984).
We observed whether the predicted slopes fell within or
outside the 95% confidence intervals of the observed SMA
regression slopes as a guide for positive or negative allom-
etry, respectively. We adjusted all P values using a Benja-
mini–Hochberg correction with an FDR Q value of 0.05 to
reduce the type I error probability across multiple compari-
sons (Benjamini and Hochberg 1995). This same statistical
protocol was used to test the hypothesis that prey size varied
with bite force. We tested whether the relationship between
prey size and moray head length or bite force was signifi-
cantly different from our isometric predictions to determine
whether larger bite force facilitates access to larger prey and
whether larger morays were consuming larger prey. To do
this, we used the prey size data extracted from the stomachs
of individuals that closely matched the sizes of morays from
when we measured invivo bite force.
We then tested the prediction that morays exhibit an
ontogenetic shift in average prey size. Since morays exhibit
morphological adaptations for consuming large prey, we
wanted to establish the range of maximum and minimum
prey sizes across moray ontogeny. To do this, we adopted
an approach by King (2002) which further uses regres-
sions to examine the upper and lower bounds of prey. We
first used ordinary least squares regression (OLS) of log-
transformed moray head length and log-transformed prey
standard length to determine the relationship between the
two variables. Then, we analyzed the variation in data sur-
rounding the regression by examining only positive and then
only negative residuals. We ran subsequent OLS regressions
for data points falling above the regression line (points with
positive residuals) and those data below the regression line
(points with negative residuals) to determine whether the
lines forming the upper and lower bounds of prey size were
significantly different from a slope of 0. Slopes that were
significantly different from 0 suggest that maximum and
minimum prey size increases with moray size.
Results
Gut contents
Between 2012 and 2016, we trapped 1338 moray eels across
our six trapping sites (Fig.1). From these morays, we iso-
lated 169 distinguishable dietary items from the stomachs of
196 G. mordax (14.6%). The proportion of trapped morays
with food in their stomachs varied little from 2013 to 2016
(16–17%). Ironically, in 2012, we trapped the most morays,
but retrieved the least amount of dietary items (8%).
During our 5years of trapping, ~ 72% of the morays with
stomach contents contained only a single dietary item in
their gut. The most we recovered from a single moray was
four kelp bass (Paralabrax clathratus). Moray diet consisted
mainly of fish (range: 69–95%), with kelp bass as the most
frequently consumed prey item (range: 63–297mm, LT;
Fig.3). On average, kelp bass composed ~ 64% of the dietary
items recovered (range over the years: 40–93%). ANOVA
Fig. 3 Size range of kelp bass consumed (N = 81) by G. mordax
(shaded area) relative to reported size range of the species. Total size
range of kelp bass was from data reported in Young, 1963. The repro-
ductive maturity (178mm LT) and most frequently consumed dietary
items of kelp bass relative to size are overlaid (data from Quast, 1968)
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880 Oecologia (2018) 188:875–887
1 3
revealed that the average size of consumed kelp bass var-
ied across years (p <0.0001; df = 4; F = 12.75). A Tukey’s
post hoc test showed that the average size of kelp bass that
morays consumed in 2015 (103mm) was significantly
smaller than those consumed in 2014 (140mm; p <0.0001),
2016 (135mm; p < 0.05), and 2012 (172mm; p < 0.0001).
However, mean kelp bass size consumed in 2015 and 2013
was not significantly different (p > 0.37).
The second and third most frequently consumed items
were red rock shrimp (Lysmata californica) and two-spotted
octopus (Octopus bimaculoides), respectively (Supplemen-
tary Table1). Harder prey items such as kelp crab (Pugettia
productus) and California spiny lobster (Panulirus interrup-
tus) were also retrieved from the stomachs; however, these
items were typically on the smaller end of the size range for
the species (< 100mm) and infrequently consumed (8 times
over 5years; ~ 5% of all dietary items). Two mantis shrimp
(Hemisquilla ensigera) were recovered from the stomachs
of morays (in 2013 and 2016), and a single blind goby
(Typhlogobius californiensis) was recorded in 2015. Other
notable dietary items include juvenile garibaldi (Hypsypops
rubicundus), blacksmith (Chromis punctipinnis), and con-
specifics; cannibalism was only observed in 2015 and 2016
(TableS1). The number of prey items consumed did not
vary across years (Kolmogrov–Smirnov test, 0.09 < p < 0.7).
Similarly, no significant difference was detected between the
proportions of different types of prey items (kelp bass, mixed
fishes, crustaceans, and molluscs) consumed across years
(Kolmogrov–Smirnov test, 0.09 < p < 0.94).
We binned morays into four-size categories and looked
for patterns between moray size categories and the known
size range of kelp bass consumed across years (Fig.4).
While at least one individual from all size categories was
represented across the 5years, the most common size cat-
egory of moray for which we removed stomach contents
was the 75–106mm LH category. In 2015, stomach contents
from multiple individuals from all four-size categories were
represented.
Dietary habits: specialist orgeneralist
Although linear selectivity index values (L) varied across
years (Fig.5), kelp bass consistently exhibited the highest
L relative to other items in the habitat in all years except
2013 L range = 0.84–0.17; L in 2013 = 0.17). Two-spotted
octopus exhibited the highest L in 2013 (0.25). Red rock
shrimp L range = 0.04 (2012)–0.18 (2013) and two-spotted
octopuses L range = 0.03 (2014)–0.25 (2013) were the only
other dietary items that displayed consistent positive L val-
ues across years. We found that morays did not consume
the most commonly occurring species in the environment.
Although blacksmith was the most dominant vertebrate spe-
cies counted in transect surveys, these fish were infrequent
in the stomachs of morays (L range = − 0.50 to − 0.44).
Señorita (Oxyjulis californica) and California sheephead
(Semicossyphus pulcher) were also commonly observed
in the environment, but neither of these species were ever
recovered from moray stomachs. Overall, these results sug-
gest that G. mordax primarily specializes on kelp bass with
invertebrates serving as supplementary prey.
Bite force
We collected bite force measurements on 49 G. mordax
(range: 567–1192mm LT; mean: 804mm LT) during the
2015 and 2016 trapping seasons. Bite forces ranged from
32.69 to 467.69N and scaled with strong positive allometry
with most morphological measurements (mass: R2 = 0.43,
slope = 0.73; LT:R2 = 0.46, slope = 2.65); and LH:R2 = 0.46,
slope = 2.4; both p < 0.0001). Head width (Lw) was the
only morphological feature that showed a negative allo-
metric relationship with bite force (R2 = 0.42, slope = 1.71,
p < 0.0001; Fig.6). Based on the strong allometry between
bite force and head length, we tested the relationship
between prey size (SLmm) and bite force. We found no rela-
tionship between prey size and bite force in each of our prey
categories (kelp bass, p > 0.383); mixed fishes, p > 0.684;
and invertebrates, p > 0.665), suggesting that an increase in
bite force does not facilitate morays consuming larger kelp
bass, larger mixed fishes, or invertebrate prey.
Predator–prey size relationships
We measured total lengths (LT) for 125 wholly intact prey
items. The largest dietary item recovered was a kelp bass
(297mm, LT), which was consumed by the largest moray in
our data set (1195mm, LT). This kelp bass length was ~ 26%
of the moray’s total length and ~ 169% of its LH.
The smallest prey consumed was a kelp crab (11mm,
carapace length), which was extricated from a moray
measuring 692mm in LT (1.6% of the moray’s LT). There
was no relationship between moray LH and prey length
for all prey categories (kelp bass: p >0.372; mixed fishes:
p >0.644; invertebrate prey: p > 0.665). However, the
regression lines between moray LH and maximum and
minimum prey size for kelp bass significantly differed
from 0 (maximum and maximum, p <0.001), indicating
an ontogenetic shift, where maximum and minimum sizes
of kelp bass increased throughout ontogeny (Fig.7). The
regression lines for moray LH and maximum size for mixed
fishes and invertebrates also indicated slopes significantly
greater than 0 (slopes = 0.12–0.24; p < 0.001). Maximum
invertebrate size was retested without the apparent out-
lier and still returned a slope significantly different from 0
(p < 0.001). Therefore, with invertebrate prey less common
in the moray diet, this outlier remained in the data set.
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881Oecologia (2018) 188:875–887
1 3
Slopes for moray LH and minimum size for mixed fishes
(p =1) and invertebrates did not differ significantly from
0 (p = 1). These results reveal an ontogenetic telescoping
pattern for mixed fishes and invertebrate prey, but where
the minimum prey size does not increase over ontogeny.
This suggests that while larger morays do eat larger fishes
from a variety of taxa and larger invertebrates, the small-
est of these prey do not drop out of their diet as observed
with kelp bass prey.
Discussion
Functional ecology ofG. mordax
We provide the first detailed multi-year data set on diet for
G. mordax, showing that in Two Harbors, Catalina Island,
the California moray is a piscivorous predator that special-
izes on kelp bass. Furthermore, we found a clear pattern of
ontogenetic shift for kelp bass, where maximum prey size
024 6
8
10 12 14 16 18 20
Kelp bass
Crustaceans
Mollusks
Mixed fishes
UnID fish
2016
2015
2014
2013
Proportion of dietary item (%)
2012
LH
L
H
L
H
L
H
L
H
L
T
Fig. 4 Bars represent the contribution of five prey categories to the
diet of G. mordax. Each bar reflects diet data for a single year. Kernel
density plots are displayed on the right with mean size (vertical lines)
of kelp bass consumption by LH range (mm) and age class, in paren-
theses. LH were converted to age class date following the regression
line presented in Higgins etal. (2017)
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882 Oecologia (2018) 188:875–887
1 3
-1
-0.8
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
0.8
1
Blacksmith
(0;2071)
CA moray
CA spiny
lobster (0;7)
Cr. urchin
(0;95)
Garibaldi
(0;39)
Kelp bass
(14;418)
Kelp crab Kelpfish RR shrimp
(1;0)
Rockfish
spp. Rock wrasse
Senorita
(0;683)
Sheephead
(0;120)
Striped
kelpfish Two-spotted
octopus
2012
-1
-0.8
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
0.8
1
Blacksmith
(1;1537)
CA moray CA spiny
lobster
(1;11)
Cr. Urchin
(0;90) Garibaldi
(0;99)
Kelp bass
(19;415)
Kelp crab Kelpfish RR shrimp
(14;0)
Rockfish
spp. (3;0) Rock wrasse
Senorita
(0;164)
Sheephead
(0;114)
Striped
kelpfish
(1;0)
Two-spotted
octopus (1;0)
2013
-1
-0.8
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
0.8
1
Blacksmith
(0;1387)
CA moray CA spiny
lobster
Cr. urchin Garibaldi
(2;117) Kelp bass
(22;299)
Kelp crab Kelpfish RR shrimp
(2;0) Rockfish
spp.
Rock wrasse
(0;125)
Senorita
(0;274)
Sheephead
(0;118)
Striped
kelpfish
(3;0)
Two-spotted
octopus (1;0)
2014
-1
-0.8
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
0.8
1
Blacksmith
(1;1858)
CA moray
(2;0)
CA spiny
lobster
Cr. Urchin
(0;288) Garibaldi
(3;224)
Kelp bass
(34;378)
Kelp crab Kelpfish RR shrimp
(5;0)
Rockfish
spp.
Rock wrasse
(0;154)
Senorita
(0;49)
Sheephead
(0;200)
Striped
kelpfish
(1;0)
Two-spotted
octopus (6;0)
2015
-1
-0.8
-0.6
-0.4
-0.2
0
0.2
0.4
0.6
0.8
1
Blacksmith
(6;1185)
CA moray CA spiny
lobster (3;8)
Cr. urchin
(0;34)
Garibaldi
(0;116)
Kelp bass
(22;158)
Kelp crab Kelpfish RR shrimp
(3;0)
Rockfish
spp. (1;0)
Rock wrasse
Senorita
(0;253)
Sheephead
(0;94)
Striped
kelpfish
(1;0)
Two-spotted
octopus (3;0)
2016
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883Oecologia (2018) 188:875–887
1 3
increases with moray size, but small prey are dropped from
the diet of larger individuals (King 2002; Arnold 1993).
However, the inclusion of secondary and typically smaller
prey items in the stomach such as mantis shrimp, spiny
lobster, blind gobies, and red rock shrimp suggests that
morays are also opportunistic in their feeding behaviors.
Supporting this idea is our finding that crustaceans were
the most consumed prey item in 2013 when kelp bass were
not abundant.
The inclusion of small mixed fishes and crustaceans in
the stomachs of even the largest morays also supports the
idea that individuals may be somewhat opportunistic about
prey and their relative sizes. The previous studies on preda-
tor–prey dynamics in fishes reveal that, contrary to the pre-
dictions of optimal foraging models (see Ivlev 1961; Harper
and Blake 1988), patterns of prey size consumption by pred-
ators do in fact include the retention of smaller prey despite
larger predator sizes (Juanes and Conover 1995; Scharf etal.
2000). One hypothesis for why larger fish predators continue
to consume small prey is that the importance of size-depend-
ent capture success and differential encounter probabilities
outweighs that of handling time (Scharf etal. 2000). Moreo-
ver, the abundance of small prey within the system may be
significantly greater than those of larger prey, further elevat-
ing the likelihood of encounters between large predators and
small prey (Scharf etal. 2000). This may in part help explain
why we observed significantly smaller kelp bass sizes con-
sumed in 2015 relative to all other years, where they had the
largest L value. During the entirety of 2015, Santa Catalina
Island was enveloped by the strongest El Niño since 1983
(Higgins etal. 2017). This resulted in a complete loss of
kelp canopy cover (B.H., C.L. and R.M., pers. obs.) that
kelp bass use for refuge during daytime hours (Ebeling and
Bray 1976). Thus, kelp bass recruits that typically took ref-
uge in the water column likely had to hide within the reef,
thereby increasing the encounter rates between small kelp
bass and morays. In years, where smaller kelp bass may not
be as abundant, morays could function as stabilizing preda-
tors by opportunistically consuming a wide range of prey
in a frequency-dependent regime, as we observed with the
increasing, although not significant, proportion of inverte-
brate prey in the moray’s diet in 2013. These findings have
strong ecological significance for the community as a whole,
because a functional specialist such as G. mordax, provides
a mechanism for maintaining elevated biodiversity through
compensatory mortality (Connell 1978).
Predator andprey size shifts acrossyears
While the proportion of prey in the diet of the California
moray did not vary significantly across years, we found
annual differences in the average size of kelp basses con-
sumed. The average size of kelp bass consumed was smallest
in 2015, whereas the average size of kelp bass consumed was
largest in 2012. These averages are just below the reproduc-
tive size of kelp bass (Fig.3). Over the course of the 5-year
study, we observed that moray predators of a wide size range
were consuming kelp bass (Fig.4). Despite the size varia-
tion in morays, there was strong overlap in kelp bass size. In
our previous study, the distribution and abundance of moray
sizes were uneven across different coves within Two Har-
bors, Catalina Island. The largest morays were trapped only
in coves with east/northeastern-oriented faces (Higgins and
Mehta 2017). Therefore, morays originating from different
trapping sites that displayed different size structuring would
all be consuming kelp bass prey of similar sizes. In addition,
size-based predation frequencies across years may have been
determined by fluctuations in reproductive output of kelp
bass which would then lead to varying strengths of kelp bass
recruitment pulses.
Bite force andpredation pressure
Within fishes that utilize biting as the primary mechanism
to capture and consume prey, the size of the gape is often
the factor that limits the types and sizes of prey that can
be exploited (Kardong 2014). Constraints in cranial growth
and/or morphological adaptations, however, often limit the
biting ability and, therefore, may prohibit access to different
prey species or prey items of a particular size (Herrel etal.
2006; Bulté etal. 2008; Santana etal. 2010; Pfaller etal.
2011). In this study, we found that morays exhibited a rela-
tively high range of bite forces for their size especially when
compared to other apex or secondary predators. For exam-
ple, insitu bite force of the sympatric and almost exclusively
durophagus horn shark (Heterodontus francisci) at a mass of
2.95kg was 160N (Huber etal. 2005). This is comparable
to our invivo bite forces recorded for a moray measuring
2.46kg (266.54N). In addition, moray bite forces increased
disproportionately as head and body increased in size, sug-
gesting that allometric increases in bite forces may enable
the oral jaws to retain larger fish prey during feeding bouts
or even provide accessibility to hard shelled prey.
Despite exhibiting allometrically increasing bite forces,
our dietary data did not support ontogenetic shifts across
all dietary items for morays. For example, morays did not
transition from a piscivorous diet to a more durophagous diet
(or vice versa) with increasing bite forces, but instead, fed
on prey items proportional to moray head length through-
out ontogeny. This hypothesis supports the previous findings
Fig. 5 Paired linear selectivity index (L) values for the dietary items
G. mordax consumed across years (black bars). Grey bars indicate L
values for those items counted (if present) by Reef Check California
survey transects. Numbers in parentheses indicate number of items
morays consumed; number of individuals Reef Check California
counted
◂
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884 Oecologia (2018) 188:875–887
1 3
that moray jaw dentition exhibited predominantly isometric
growth, suggesting that the oral teeth grow proportionately
as individuals increase in size (Harrison etal. 2017). Tooth
growth patterns help explain why similar sized items are
consumed by morays that vary widely in size as was found in
the current study. Fracture forces for hard prey such as lob-
ster and kelp crab are necessary to test the idea that allomet-
ric increases in bite forces may enable morays to consume a
wider variety (type or size) of hard shelled prey when kelp
bass recruits are not abundant.
Based on the strong allometric pattern of bite force, we
would expect larger morays to consume fishes that exceed
their head lengths. However, we found no significant rela-
tionship between prey size and moray bite force. Our results,
therefore, suggest that kelp bass size selection is not limited
by moray bite force. Rather, other variables such as encoun-
ter rates, capture rates, or handling times could limit the
sizes of kelp bass prey in the California moray’s diet. Cali-
fornia morays, similar to other morays (Miller 1987, 1989)
or eel species (Helfman and Clark 1986), are known to ram,
shake, knot, or use body rotations, to force large prey into
their mouths or to remove pieces from larger prey items. In
a previous study, we showed that prey size increased total
feeding time and prey manipulation duration when morays
were fed dead fish or cephalopod prey (Diluzio etal. 2017).
Feeding durations and energetic demands necessary to cap-
ture and handle large live prey of increasing size would
undoubtedly affect the caloric benefits of going after these
larger prey.
Frequency ofpredation
Of the morays trapped over the 5-year period, we found that
the overwhelming majority had empty stomachs (85.4%).
The previous studies have shown that piscivores have empty
stomachs more often than non-piscivores and that noctur-
nal fishes tend to run empty more often than diurnal fishes.
Piscivorous fishes that consume prey whole also tended to
have the highest proportions of empty stomachs (Arrington
etal. 2002). Our data set revealed that the California moray,
a nocturnal piscivore, infrequently turned up with stomach
contents averaging ~ 14.6% over the 5-year period in sum-
mer months. This low percentage of stomach contents could
reflect the challenge of capturing kelp bass prey as pisci-
vores tend to be less successful compared to planktivores
(Juanes etal. 2002). Capture success in piscivores has also
been shown to decrease when prey size to predator size ratio
increases (Miller etal. 1988). The challenge of capturing
y = 0.73x + 5.1
R = 0.43
0
1
2
3
4
5
6
7
-1.5 -1 -0.5 0 0.5 1 1.5
Log BF (N)
y = 2.65x - 12.65
R = 0.46
0
1
2
3
4
5
6
7
6.3 6.4 6.5 6.6 6.7 6.8 6.9 7 7.1 7.2
Log BF (N)
Log
y = 2.4x - 6.2
R = 0.46
0
1
2
3
4
5
6
7
4.2 4.3 4.4 4.5 4.6 4.7 4.8 4.9 5 5.1 5.2
Log BF (N)
y = 1.71x - 0.98
R = 0.42
0
1
2
3
4
5
6
7
2.5 2.7 2.9 3.1 3.3 3.5 3.7 3.9 4.1
Log BF (N)
Log
LHLw
LT
BA
CD
Log Mass
Log
Fig. 6 Relationships between G. mordax bite force (log) and mass
(a), total length (b), head length (c), and head width (d). All varia-
bles, with the exception of head width, display a positive allometric
relationship with bite force (R2 range: 0.42–0.46). Head width exhib-
ited a negative allometric relationship. Dashed lines represent an iso-
metric slope
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885Oecologia (2018) 188:875–887
1 3
fish prey has leaded others to speculate that maximum fishes
consumed by piscivores are often considerably smaller than
what would be predicted by predator gape size alone (Juanes
and Conover 1995; Christensen 1996). Therefore, while
predator gape size or cleithrum width may biomechanically
limit the sizes of prey a predator may ingest, the behavio-
ral abilities (i.e., evasiveness) of the prey may in fact more
tightly regulate the sizes and types of prey consumed before
gape morphology of the predator interacts with feeding.
Alternatively, California morays may have low metabolic
rates and individuals may not need to consume prey fre-
quently. Higgins and Mehta (2017) showed that the body
condition of morays was relatively consistent across moray
size categories and coves suggesting if preferred prey are
challenging to capture, it is not reflected in moray body
condition.
Trophic placement
Evidence from studies conducted in the tropics suggests that
morays are predatory fishes that can be found in densities
similar to commercially important predatory fishes such as
serranids (sea basses and groupers) and lutjanids (snappers)
(Gilbert etal. 2005) and can alter future community struc-
ture by preying upon newly settled recruiting fishes on Car-
ibbean patch reefs (Parrish etal. 1986; Carr and Hixon 1995;
Young and Winn 2003). Within the coves of Two Harbors,
G. mordax is an abundant, static, carnivorous predator (Hig-
gins and Mehta 2017; Harrison etal. 2017) that specializes
on kelp bass, but can consume a relatively wide diversity of
prey species throughout ontogeny. These results, therefore,
suggest that morays have the densities to inflict consistent
and elevated predation pressures on their prey populations
as tertiary consumers; however, metabolic data would be
necessary to understand the effects of G. mordax on vari-
ous prey populations. The California moray was previously
categorized as a secondary consumer (Graham 2004). Under
this classification, G. mordax at two harbors is grouped in
the same carnivorous fish category as their primary prey,
kelp bass. Our results, suggest that G. mordax should be
positioned above the carnivorous fishes category and is a ter-
tiary consumer alongside sharks, rays, pinnipeds, and birds.
While morays are apex consumers in tropical waters (Carr
and Hixon 1995; Page etal. 2013), we hesitate to label G.
mordax as an apex consumer without additional field obser-
vations on the habits of other resident marine predators, such
as Harbor seals, Phoca vitulina.
Acknowledgements We thank Experiment.com for our crowd funding
platform and the support we received in 2014. T. Williams, M. Carr,
J. Estes, V. Baliga, K. Dale, S. Kienle, C. Jaquemetton, and K. Voss
provided valuable input and feedback on the manuscript. We thank S.
Ciandro, Sean Hayes, Cyril Mitchell, Rachel Higgins, and Ann Marie
Osterback for providing invaluable field support; A. Diluzio, S. Eckley,
S. Burns, J. Harrison, R. Higgins and J. Redwine assisted with SCUBA
transects and data collection; We thank S. Connor, L. Oudin, T. Oudin,
K. Spafford, K. Erickson and the staff at the University of Southern
California Wrigley Institute for Environmental Studies for equipment
y = 0.22x + 1.45
R = 0.01
0
0.5
1
1.5
2
2.5
3
1.6 1.7 1.8 1.9 2 2.1 2.2 2.3
Log prey size (mm)
Log moray L
H
(mm)
y = 0.74 + 0.65
R = 0.53
2
y = 0.17 + 1.09
R = 0.01
2
y = 0.12x + 1.84
R = 0.01
0
0.5
1
1.5
2
2.5
3
1.6 1.7 1.8 1.9 2 2.1 2.2 2.3
Log prey size (mm)
Log moray L
H
(mm)
y = 0.67 + 1.03
R = 0.32
2
y = 0.05 + 1.85
R = 0.05
2
Kelp bass
Invertebrates
y = 0.24x + 1.34
R = 0.01
1.6 1.7 1.8 1.9 2 2.1 2.2 2.3
Log prey size (mm)
Log moray L
H
(mm)
y = 1.36 - 0.43
R = 0.87
2
y = 0.24 + 0.95
R = 0.07
2
0
0.5
1
1.5
2
2.5
3
Fig. 7 Degrees of ontogenetic shift (kelp bass) and telescoping
(mixed fishes and invertebrates) using the relationship between G.
mordax head length (log) and prey size (log) for kelp bass (N = 81),
mixed fishes (N = 28), and invertebrate prey (N = 16). Black lines rep-
resent the OLS regression through the entire data set for each prey
category. Thick grey lines represent OLS regression through posi-
tive and negative residual points. In all prey categories, we observe
that the slope of the relationship between prey size and head length
is significantly different from 0. Solid grey lines indicate slopes
significantly greater than 0 for prey in the maximum size category,
whereas dashed grey lines indicate slopes not significantly different
from 0. For kelp bass prey, larger morays dropped smaller prey items
from their diet that reveals an ontogenetic shift in diet, as opposed
to ontogenetic telescoping observed in mixed fishes and invertebrates
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886 Oecologia (2018) 188:875–887
1 3
and logistical support. All procedures were approved by the Institute of
Animal Care and Use Committee (IACUC) at the University of Califor-
nia, Santa Cruz, USA (#1007). This research was in partial fulfillment
of the doctoral of philosophy in the Ecology and Evolutionary Biology
Department at the University of California, Santa Cruz.
Author contribution statement RSM designed the study. RSM, BAH,
and CJL collected the data. BAH analyzed the data. RSM, BAH, and
CJL interpreted the data. BAH wrote the manuscript. RSM and CJL
provided feedback on various iterations of the manuscript.
Funding The authors are grateful to the Packard and Hellman Foun-
dation grants and UCSC’s Committee on Research grants to R.S.M.
B.A.H was in part funded by G. Gilbert and I. Parker via a UCSC
SCWIBLES GK-12 Fellowship from the National Science Founda-
tion (NSF GK-12 DGE-0947923), and by Mike Beck from the Nature
Conservancy.
Open Access This article is distributed under the terms of the Crea-
tive Commons Attribution 4.0 International License (http://creat iveco
mmons .org/licen ses/by/4.0/), which permits unrestricted use, distribu-
tion, and reproduction in any medium, provided you give appropriate
credit to the original author(s) and the source, provide a link to the
Creative Commons license, and indicate if changes were made.
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