Download Demography and feeding behavior of the kelp crab Taliepus

Invertebrate Biology 132(2): 133–144.
© 2013, The American Microscopical Society, Inc.
DOI: 10.1111/ivb.12021
Demography and feeding behavior of the kelp crab Taliepus marginatus in subtidal
habitats dominated by the kelps Macrocystis pyrifera or Lessonia trabeculata
David Jofre Madariaga,1,2 Marco Ortiz,2 and Martin Thiel1,3,a
1
2
Facultad de Ciencias del Mar, Universidad Cat
olica del Norte, Coquimbo, Chile
Instituto Antofagasta de Recursos Naturales Renovables (IARnR), Instituto de Investigaciones Oceanol
ogicas,
Facultad de Recursos del Mar, Universidad de Antofagasta, Antofagasta, Chile
3
Centro de Estudios Avanzados en Zonas Aridas,
Coquimbo, Chile
Abstract. We studied the population and feeding ecology of the kelp crab Taliepus marginatus in subtidal kelp forests dominated by either of two morphologically different kelp species (Macrocystis pyrifera or Lessonia trabeculata) in northern Chile. The sizes and
abundances of T. marginatus differed between the two kelp habitats. Kelp crabs were more
abundant in the M. pyrifera forest than in the L. trabeculata forest. Size-frequency distributions showed that juvenile and immature crabs were more common in the M. pyrifera forest
than in the L. trabeculata forest, where reproductive adults predominated. The smaller crabs
in the M. pyrifera habitat also consumed a higher proportion of kelp tissues than the larger
crabs in the L. trabeculata habitat, which had a higher proportion of animal food in their
diet. In both kelp forests, individuals of T. marginatus showed a similar pattern of nocturnal feeding over a 24-h period, consuming more food at night than during the day. The
more complex and dense forests of M. pyrifera appear to present better nursery habitats for
juvenile kelp crabs than the more open and less dense forests dominated by L. trabeculata.
These results suggest that the role of the two kelp habitats for T. marginatus varies during
the life cycle of the kelp crabs, with M. pyrifera tending to have nursery function and
L. trabeculata being more suitable as a reproductive habitat.
Additional key words: habitat use, nursery habitat, reproductive habitat, diet
Habitats differ in their availability of food items,
predation pressure, and physical disturbance (e.g., habitat-specific environmental factors), resulting in specific
costs and benefits for individuals (Amaral et al. 2008).
For example, habitats with higher structural complexity offer more shelter and resources, thereby supporting high densities of individuals. On the other hand,
high densities may result in interference competition
for resources and space, leading to emigration and
occupation of less favorable habitats by some individuals, allowing for more feeding time, albeit possibly on
less preferred food items (Amaral et al. 2008).
Kelp beds are highly productive benthic ecosystems (V
asquez 1992; Steneck et al. 2002; Ortiz
2008), which provide shelter for a wide variety of
species (e.g., fishes, seastars, crabs, and snails) with
different feeding behaviors (Smith et al. 1996). Majid crabs living on kelps act as both consumers and
a
Author for correspondence.
E-mail: [email protected]
prey, and thus represent an important trophic link
(Hines 1982). As consumers, they obtain most of
their nutrition from algal material (Hines 1982;
Kilar & Lou 1986; Daly & Konar 2010). The nutritional value and abundance of this algal material
are factors that determine its consumption (Wolcott
& O′Connor 1992), and multiple structural and
chemical adaptations have evolved that might
reduce the palatability of seaweeds (Duffy & Hay
1990). Despite this, some herbivores from temperate
kelp beds consume large amounts of algal biomass
(Leighton 1966; Vasquez & Buschmann 1997).
Some algal consumers, primarily the smaller, less
mobile ones, commonly specialize in one type of
food (e.g., the habitat-forming macroalgae) and live
directly on it, using it as both food and shelter
(Hines 1982; Woods 1993; Stachowicz & Hay 1999;
Gutow et al. 2012). In contrast, larger individuals
that roam farther also incorporate other food items
in their diet. This may lead to spatial segregation
between different ontogenetic groups.
134
In many habitats, crab consumers have special
feeding rhythms to avoid interspecific competition
for food and predation risk (Jesse 2001; KronfeldSchor & Dayan 2003). For example, members of
many brachyuran species feed mainly during the
night, with no or low foraging activity during the
day (Aris et al. 1982; Jesse 2001; Novak 2004;
Almeida et al. 2008). By limiting their activity period to times of low predation pressure, these crabs
reduce the amount of time available for foraging
(Aris et al. 1982).
Taliepus marginatus (BELL 1835) (Superfamily
Majoidea) is a decapod crab widely distributed
along the Chilean coast, but little is known about
its life cycle. Recently settled juveniles of its congener T. dentatus (MILNE EDWARDS 1834) are commonly found in shallow subtidal habitats, often
dominated by turf algae, and while the habitats of
growing juveniles and subadults are not known, the
reproductive adults generally occur in subtidal kelp
forests (Pardo et al. 2007; Palma et al. 2011). Taliepus marginatus has been reported from deeper subtidal waters (Antezana et al. 1965) in subtidal kelp
systems dominated by either Macrocystis pyrifera
(LINNAEUS) C. AGARDH 1820 or by Lessonia trabeculata VILLOUTA & SANTELICES 1986 (Villegas et al.
2008). These two kelp species show important differences; they develop in different environmental
conditions, have contrasting morphological structures (Ortiz 2008; Villegas et al. 2008), and likely
differ substantially in their tissue consistency and
attractivity for grazers (for differences between M.
pyrifera and Lessonia spp. see for example Pansch
et al. 2008). Based on these ecological differences,
we expected that the natural diet, density, size distribution, and foraging activity of T. marginatus
might differ between these two kelp habitats. Specifically, we hypothesized that smaller crabs would be
more common in the shallow and dense kelp beds
of M. pyrifera, while larger crabs would dominate
in the deeper and more open beds of L. trabeculata.
We also expected to find differences in the feeding
ecology of crabs between the two kelp systems.
This study thus aims to contribute to knowledge
of the demography and feeding ecology of T. marginatus in two subtidal kelp habitats. The objectives
were to compare the (i) size structure, (ii) density,
(iii) natural diet, and (iv) daily feeding cycle of T.
marginatus inhabiting beds dominated by either M.
pyrifera or L. trabeculata. This work is part of an
extensive study examining the properties of the kelp
forest ecosystems formed by M. pyrifera and L. trabeculata (Ortiz 2008, 2010).
Invertebrate Biology
vol. 132, no. 2, June 2013
Jofre, Ortiz, & Thiel
Methods
Study area
This study was carried out in austral fall during
the months of April 2006 and April 2007 near Isla
Santa Marıa at the southern tip of the Mejillones
Peninsula (SE Pacific coast, Antofagasta, Chile:
23°27′S–70°36′W). The study area is close to an
important upwelling center that supplies nutrients to
the coastal ecosystem (Escribano et al. 2004). These
nutrient-rich coastal areas are dominated by subtidal
kelp forests of Macrocystis pyrifera and Lessonia
trabeculata, which develop in different environmental conditions (Ortiz 2008). Macrocystis pyrifera
forms extensive and complex patches in coastal
areas mostly protected from direct wave exposure,
where they often grow on boulders extending over
depths of 2–10 m (Vega et al. 2005; Villegas et al.
2008). Blades of M. pyrifera grow along the entire
stipe, forming a dense mesh of algal canopy from
the bottom to the sea surface (Villegas et al. 2008).
In contrast, L. trabeculata grows mostly on more
exposed coasts on bedrock ranging in depth from 8
to 14 m (Vega et al. 2005; Villegas et al. 2008). The
blades of older kelp stands usually originate from
the stipes at some distance above the bottom, but
the individual kelp plants rarely exceed 1.5 m in
height and thus do not reach the sea surface. Given
their different bathymetric distribution, at the study
site the kelp forests composed of M. pyrifera are
closer to the shore, growing over a gentle slope
down to ~6 m depth, while stands of L. trabeculata
start at the seaward edge of the M. pyrifera patches,
extending in depth from ~5 m down to ~12 m
(Fig. 1).
Both kelp forests have a high standing biomass,
but system throughput (a measure of ecosystem
metabolism) in M. pyrifera kelp beds is higher than
in L. trabeculata (Ortiz 2008, 2010). A wide diversity
of different invertebrates is found in the kelp forests
around Isla Santa Marıa; among these, sea urchins
and their seastar predators dominate in biomass
(Vasquez et al. 2006; Gaymer et al. 2010). Fish predators are also important in these kelp forests (Ortiz
2008), which offer more refuge and food than surrounding barren grounds (e.g., Vasquez et al. 2006;
Villegas et al. 2008; Perez-Matus et al. 2012).
In these kelp systems, Taliepus marginatus is one
of the most abundant brachyuran crabs. Settlement
occurs primarily during austral spring (personal
observations), and growing juveniles and subadults
were expected to be most abundant during late
Demography and feeding behavior of a kelp crab
135
Fig. 1. Location of the study area on the Mejillones Peninsula close to Santa Marıa Island, SE Pacific coast (northern
Chile), showing Macrocystis pyrifera (dark shading) and Lessonia trabeculata (light shading) kelp forests. Sampling
plots in each kelp habitat are shown.
summer and fall, as had also been reported for
other kelp inhabitants (Gaymer et al. 2010) and for
kelp crabs in California (Hines 1982). Consequently,
sampling of crabs was conducted during early austral fall (April). Crabs collected during the fall of
two subsequent years (2006 and 2007) were pooled
herein.
Sampling procedure
To estimate abundance and size structure of the
crabs in the two kelp habitats, we collected samples
of T. marginatus from three rectangular plots of
20 m2 (592 m) in each kelp forest (Fig. 1). The
positions of these sampling plots were selected from
the areas with the highest kelp density, covering the
main depth range of each kelp. In the M. pyrifera
forest one of the three rectangular plots was placed
close to the shore (~3 m deep) and the other two
were oriented away from shore (~5–6 m deep), and
in the L. trabeculata forest the plots were placed
between 8 and 12 m depth. All rectangular plots
were linked and fixed by an anchor in the middle
(Fig. 1). Each plot was carefully sampled by two
scuba divers using semiautonomous (hookah) diving
systems. The scuba divers collected crabs on the
bottom and in the kelp canopy by carefully surveying the entire fronds (e.g., searching on both sides
of the blades). This was done to collect all crabs
>10 mm carapace width (CW), including those that
were still camouflaged against the canopy background. Crabs were collected by hand and placed
into thick-walled plastic bags with handles. These
plastic bags were used because kelp crabs quickly
entangle in the mesh of regular dive bags. At the
end of each sampling, all crabs were transported to
the shore for further processing. To preserve the
stomach contents, each crab was injected with a
solution of 10% formalin in the oral and abdominal
regions. This method was used to rapidly stop digestion and degradation processes. All samples were
frozen (20°C) for subsequent analysis.
Sample analysis
In the laboratory, all crabs were identified as T.
marginatus according to Retamal (1977). Sex was
determined through visual observation of the abdomen. Females were distinguished by a wide abdomen, and all mature females were examined for
Invertebrate Biology
vol. 132, no. 2, June 2013
136
brooded embryos. The total wet weight of each crab
was measured with a semianalytical balance
(precision0.1 g). Carapace width (CW) was measured with a digital caliper (precision0.1 mm). In
this study, we distinguish two size groups of crabs,
juveniles and subadults (10.0–40.0 mm CW), and
adult crabs (>40.0 mm CW). The smallest ovigerous
female had a CW of 44.8 mm, suggesting that T.
marginatus reaches sexual maturity at ~40 mm CW.
The cardiac stomachs were extracted from each
specimen and the wet weights of the full (before
removing stomach contents) and empty stomachs
were measured after absorbing excess water with
paper tissues. Stomach contents were diluted in distilled water and 10% ethanol and analyzed visually
with the aid of a binocular microscope. The contents of each stomach were classified to the lowest
possible taxonomic level. Finally, the importance of
each food item in the diet of T. marginatus was
described in two ways: (i) frequency of occurrence,
and (ii) the wet weight of each food item. The frequency of occurrence was estimated based on the
presence of a particular item in the stomach using
equation (1),
ni
Fi ¼
N
where ni is the number of occurrences (number of
stomachs in which the prey i is present) and N is the
total number of stomachs containing food. Then,
each frequency was multiplied by 100 and expressed
as percentage of occurrence (%). A total of 361
crabs were examined in the two kelp habitats (258
in M. pyrifera and 103 in L. trabeculata) for frequency of occurrence. For the wet weight proportions, a total of 181 stomachs (97 from M. pyrifera
and 84 from L. trabeculata) were randomly selected
from the 361 examined stomachs (Table 1). For this
analysis, all food items (by category) were weighed
on an analytical balance (precision0.0001 g), and
the abundance of each item in each gut expressed as
a percentage of total stomach content weight. The
combination of the two methods was used to (i)
determine whether food items were present in the
diet of crabs, and (ii) estimate the proportional wet
weight (importance) of each food item in the
stomachs.
Daily feeding cycle
To determine the daily feeding cycle over 24 h,
we collected specimens of T. marginatus (n=20) at
regular intervals of 6 h (16:00, 22:00, 04:00, 10:00).
Each sampling was conducted by two scuba divers.
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Jofre, Ortiz, & Thiel
The crabs were collected by hand and placed in
thick-walled plastic bags with a handle. The divers
rapidly collected all visible crabs >40 mm CW,
because crabs had to be collected quickly at the
defined sampling hours. During the nocturnal samplings it was necessary to use a lantern, and the
restricted field of view limited the search efficiency
of divers. For this reason it was decided to focus on
larger crabs for both the day and the night samples
of the daily feeding cycle. These samples were preserved and analyzed as described above. The feeding
periodicity of T. marginatus in each kelp forest was
assessed by calculating the relative stomach content
(SC%) over a 24-h cycle by equation (2):
SCð%Þ ¼
gut content (g)
100
body weight (g)
This index describes the stomach fullness for each
sampling hour (Jesse 2001; Baumann & Kwak
2011).
Statistical analyses
Prior to analyses, all data were tested for normality using Kolmogorov–Smirnov and Shapiro–Wilk’s
tests. Homogeneity of variances was tested with Ftests or with Fligner–Killeen tests. If assumptions
were not met, data were transformed or a nonparametric test was applied (Zar 1996). To examine the
differences in the median size distribution between
kelp habitats, a nonparametric Mann–Whitney
U-test was performed. Density data were log-transformed and a t-test was used to examine the
differences in crab densities between habitats. To
determine whether the proportion of ovigerous
females differed between kelp habitats, a chi-squared
test (v2) was used. Sizes of ovigerous females from
the two kelp habitats were compared with a
Student’s t-test.
A two-way ANOVA was used to test for significant differences in the daily feeding cycle, with the
two factors being time (hour) and site (habitat).
When the ANOVAs revealed significant differences,
a post hoc Tukey HDS was applied. The analyses
were carried out using R (R Development Core
Team 2010).
Nonmetric multidimensional scaling (nMDS) was
performed to assess similarity/dissimilarity in diet
(species/taxa: using the proportion of wet weight per
food item) between habitats (Macrocystis/Lessonia)
and size groups of the crabs (10.0–40.0 mm/
>40.0 mm CW) based on the Bray–Curtis similarity
index. Prior to the analysis, the data were square-
Demography and feeding behavior of a kelp crab
Table 1. Volume proportions (%, meanSD) of each
food category (wet weight in g) in the stomach contents
of Taliepus marginatus from the two kelp habitats. Dashes
indicate absence of the respective food type in the analyzed stomachs.
Habitats
Stomachs analyzed
Food category
Macrocystis
Lessonia
Rhodophyta
Hydrozoa
Detritus
Crustacea
Mollusca
Bryozoa
Gastropod egg capsules
a
Macrocystis
(n=97)
%
Lessonia
(n=84)
%
96.35.9
—
2.43.6
0.10.4
0.10.7
0.63.7
0.10.8
a
0.1
0.11.0
—
93.913.3
5.012.2
a
0.1
0.72.0
—
0.11.3
a
0.1
a
0.1
0.1=Weight < 0.1 g.
root transformed. Three separate one-way analyses
of similarity (ANOSIM) were performed to test the
following hypotheses: (A) there are no differences in
diet composition of T. marginatus from M. pyrifera
and L. trabeculata habitats, and (B-i & B-ii) within
each kelp habitat (i & ii) there are no differences in
diet composition between immature and adult crabs.
In addition, the SIMPER routine was used to establish which species/taxa contributed most to either
the similarity or dissimilarity between habitats and
habitat per size (Clarke 1993). The multivariate
analysis was carried out using PRIMER v.6 (Clarke
& Gorley 2006).
137
Results
Size distribution and abundance
The size distribution of crabs differed significantly
between the two kelp habitats (U=28185.5; df=1;
p<0.001), even though the range of crab sizes was
similar in the two habitats (Fig. 2). The size distribution of females and males in Macrocystis pyrifera
varied from 14.0 to 63.9 mm CW (49.716.2 mm;
meanSD) and 10.9–91.3 mm (48.39.2 mm),
respectively (Fig. 2). In contrast, in Lessonia trabeculata,
females
ranged
20.9–72.2 mm
CW
(53.48.4 mm) and males ranged 10.7–97.6 mm
(70.618.4 mm) (Fig. 2). The total crab densities
were 3.11.6 ind. m2 in M. pyrifera, and 0.70.6
ind. m2 in L. trabeculata; these densities differed
significantly between the two kelp habitats (t=4.38;
df=12; p<0.001).
The proportion of females and males was 49.7%
and 50.3%, respectively, in the M. pyrifera habitat,
and 28% of all females found in M. pyrifera were
ovigerous. In the L. trabeculata habitat, the proportion of females and males was 38.3% and 61.7%,
respectively, and 66% of the females were ovigerous.
The sizes of ovigerous females did not differ significantly between the two kelp habitats (Macrocystis,
n=52; Lessonia, n=27) (t=2.027; df=77; p=0.05). The
proportion of ovigerous females was significantly
higher in L. trabeculata than in M. pyrifera
(v2=21.263; df=1; p<0.001).
Diet composition
In general, crabs from both habitats had similar
diets, but they differed in the proportional occurrence
Fig. 2. Size-frequency distribution of Taliepus marginatus in both kelp habitats. Open bars show the total frequency of
males and females in both habitats. Black bars show the frequencies of ovigerous females. Data from both study years
(April 2006 and April 2007) were pooled.
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vol. 132, no. 2, June 2013
138
Jofre, Ortiz, & Thiel
Fig. 3. Diet composition expressed as frequency of occurrence (as % of individuals) for Taliepus marginatus of two different size ranges (carapace width in mm) in each kelp habitat. n, number of stomachs examined per size range.
of kelp tissues and other types of food (Fig. 3).
Kelp remains (either M. pyrifera or L. trabeculata)
were found in the stomachs of all crabs. Tissues of
red algae were also common (~70% of all samples)
in crab stomachs, except for the small crabs in L.
trabeculata. The most common red algal genera
occurring in stomach contents were Chondrus, Chondria, Polysiphonia, Callophyllis, Pterosiphonia, Cryptopleura, and Gastroclonium. Remains of a wide
range of other taxa were also detected, particularly
Hydrozoa, Mollusca (small pieces of gastropod
shells and bivalves, including occasionally complete
individuals of Brachidontes granulatus (HANLEY
1843), Bryozoa, Polychaeta, Crustacea (parts of
carapaces, pleopods, small shrimps, and amphipods), and egg capsules of neogastropods (Mitrella
unifasciata (SOWERBY 1832), Nassarius sp., and
Crassilabrum crassilabrum (SOWERBY 1834)) (Fig. 3).
Kelp tissues (M. pyrifera and L. trabeculata) were
highest in proportional volume (96.35.9 and
93.913.3) of the stomach contents for crabs from
both kelp habitats, followed by red algae and other
items (Table 1). In both kelp habitats, all individuals
of the two crab size categories (10.0–40.0 mm and
>40.0 mm) had kelp tissues in their stomachs
(Table 2). The small crabs (10.0–40.0 mm) from L.
trabeculata had no animal tissues in their stomachs,
while all other crabs, including the small crabs from
M. pyrifera, also had ingested animal food. Diet
composition significantly differed between crabs
from both kelp habitats (ANOSIM, R Global=0.93;
p<0.001) (Fig. 4). Within each habitat, the diet composition of small crabs (10.0–40.0 mm) also differed
from that of the larger crabs (>40.0 mm); this difference was highly significant both in M. pyrifera
(ANOSIM, R Global=0.68; p<0.001) and in L. trabeculata (ANOSIM, R Global=0.66; p<0.001) (Fig. 4).
The SIMPER routine showed that the two kelp species contribute most to the dissimilarity in diets
between habitats and size categories (Table 3A,B).
Daily feeding cycle
Taliepus marginatus showed a mostly nocturnal
daily feeding cycle in both habitats (Fig. 5). There
were no significant differences in feeding patterns
Table 2. Percentage of individuals of Taliepus marginatus per size class with algal tissues and other kinds of food (animal tissue and detritus) in the stomach contents, in both kelp habitats.
Habitats
Macrocystis
Size range in mm (sample size)
Percentage of crabs with algal tissue
Percentage of crabs with other tissue
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vol. 132, no. 2, June 2013
Lessonia
10.0–40.0 (n=67)
>40.0–92.0 (n=191)
10.0–40.0 (n=14)
>40.0–92.0 (n=89)
100%
31%
100%
46%
100%
0%
100%
58%
Demography and feeding behavior of a kelp crab
139
Fig. 4. Nonmetric multidimensional scaling (nMDS) plot, resulting from classification analysis (Bray–Curtis similarities) based on the wet weight (g) of item food (taxa/species) of Taliepus marginatus collected from Macrocystis pyrifera
(circles) and Lessonia trabeculata (triangles). Data were square-root transformed for analysis. Open dots and triangles
represent immature crabs, filled dots and triangles represent mature crabs. Number of crabs analyzed per habitat: M.
pyrifera, n=97, and L. trabeculata, n=84. For SIMPER details see Table 3.
between the two kelp habitats (Fig. 5, Table 4). In
M. pyrifera, the peak stomach fullness was reached
at 22:00, remained high until 4:00, and then
decreased until 10:00. In L. trabeculata the feeding
pattern was similar, but the peak stomach fullness
was reached at 4:00, after which it decreased sharply
Table 3. Results of SIMPER analysis of (dis)similarity in diet composition (A) within and between habitats, and (B)
between immature and adult crabs (size ranges in mm, CW) from each kelp habitat (i & ii). Based on wet weight of
food items (g wet weight per food item) from the stomach contents of Taliepus marginatus. Av. Biomass=mean biomass, Contribution %=contribution percentage of each taxon, Av. Diss.=average of dissimilarity, and Av. Sim.=average of similarity.
Av. Biomass (g ww)
A. Habitats
Between habitats (Av. Diss.=95.75)
M. pyrifera
L. trabeculata
Rhodophyta
Within habitats
Macrocystis (Av. Sim.=76.07)
Lessonia (Av. Sim.=68.77)
B. Crab sizes (range mm)
ii-a. Macrocystis (Av. Diss.=43.40)
M. pyrifera
Rhodophyta
Crustacea
ii-b. Lessonia (Av. Diss.=59.63)
L. trabeculta
Rhodophyta
Contribution
%
Macrocystis
Lessonia
n=97
n=84
1.15
0
0.12
0
1.13
0.18
95.14
42.91
6.96
1.13
93.84
93.38
1.15
10.0–40.0
n=14
0.54
0.06
0.05
n=12
0.37
0
>40.0–92.0
n=83
1.25
0.13
0.01
n=72
1.25
0.22
74.15
11.92
5.93
77.96
15.54
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140
Jofre, Ortiz, & Thiel
observed in adult crab stomachs may provide
energy for reproductive purposes. Overall, these
results suggest that the role of the two kelp habitats for T. marginatus varies during the life cycle
of the kelp crabs, with M. pyrifera tending to have
nursery function and L. trabeculata being more
suitable as reproductive habitat.
Habitat use
Fig. 5. Relative stomach contents (in % body wet weight)
of Taliepus marginatus over a 24 h cycle in each kelp habitat. Means and standard deviation (vertical bars) calculated from 20 crab samples at each sampling hour.
Different letters indicate significant differences (p<0.001)
between sampling hours. For ANOVA details see
Table 4.
Table 4. Results from the statistical analysis of relative
stomach content volume (SC%) using two-factor analysis
of variance (ANOVA), with the factors Time (hour:
16:00, 22:00, 4:00, and 10:00) and Site (habitat: Macrocystis and Lessonia).
Source
df
MS
F value
p-value
Hour
Habitat
Hour: Habitat
Residuals
3
1
3
152
11.262
1.886
1.448
0.493
22.808
3.820
2.934
<0.001
0.052
<0.05
until the morning (10:00). In both kelp habitats, the
two night samplings differed significantly from the
day samplings (Fig. 5, Table 4).
Discussion
The size distribution of the kelp crab Taliepus
marginatus differed between kelp forests dominated
by Macrocystis pyrifera and Lessonia trabeculata.
While the higher abundance, especially of smaller
crabs, in M. pyrifera forests suggests that this kelp
could favor the survival and growth of juvenile
and subadult crabs, the higher proportion of large
males and of ovigerous females in L. trabeculata
indicates that this kelp species has an important
reproductive function for T. marginatus. In both
kelp habitats, kelp tissues were the most abundant
food item of T. marginatus, but adult crabs (and
small crabs in M. pyrifera) also ingested other food
items. The larger proportion of animal food
Invertebrate Biology
vol. 132, no. 2, June 2013
Many decapod crustaceans have changing habitat
requirements during their life cycle. Our field data
showed differences in the size distribution and density of T. marginatus between the two kelp habitats,
which can be attributed to two possible causes.
First, the two kelp species differ in habitat structure
(Vega et al. 2005; Villegas et al. 2008), and second,
the M. pyrifera kelp forests, due to their density,
complexity, and proximity to the coast, could play
an important role as nursery habitat for smaller
crab individuals. In a field study on the most conspicuous and abundant brachyuran species inhabiting the shallow rocky subtidal zone in central Chile,
Pardo et al. (2007) found that settlement and
recruitment of T. dentatus (the congener of T. marginatus) occurred mainly on shallow subtidal algal
turfs. Furthermore, they could not find larger juveniles in any of the habitats surveyed (e.g., algal turf,
cobbles, and shell hash). This might be due to an
ontogenetic habitat shift from turf algae to adjacent
kelp forests. Small recruits find shelter and protection in shallow subtidal seaweeds (Pardo et al.
2007), which even may offer chemical defenses
against fish predators (Palma et al. 2011).
Rockfishes are presumed the major predators of settlers and juveniles of most invertebrates in these
kelp habitats (Fari~
na et al. 2008). Given the complex structure of M. pyrifera forests, juvenile crabs
might escape predation in this habitat, enhancing
their recruitment, as also reported for other invertebrate species inhabiting this kelp (Almanza et al.
2012).
The presence of the largest (and mostly reproductive) individuals of T. marginatus in the deeper
(seaward) L. trabeculata kelp forests has also been
reported by Palma et al. (2011), supporting our
interpretation that this kelp has an important
reproductive function for kelp crabs. Similar observations have also been reported for Pugettia producta (RANDALL 1840) from California kelp forests
(Hines 1982; Hultgren & Stachowicz 2010). The
size distribution of P. producta varies from the low
intertidal zone (Mastro 1981) to the deeper sections
of the kelp forest (Hines 1982). Individuals of this
Demography and feeding behavior of a kelp crab
species are apparently recruiting into intertidal
Phyllospadix zones, and subsequently migrate into
the subtidal kelp forests (Hines 1982). Several studies on P. producta point out that adult crabs (52–
72 mm CW) prefer kelps as reproductive habitat
(Hines 1982; Wicksten & Bostick 1983; Hultgren &
Stachowicz 2010). Therefore, the predominance of
small recruits in nearshore habitats (turf algae, seagrass, cobble) and of reproductive individuals in
the seaward, deeper kelp habitats might be a general pattern for kelp crabs (Hines 1982; Hultgren
& Stachowicz 2010; Palma et al. 2011; this study).
The ultimate causes (e.g., food availability, shelter,
lower competition, larval dispersal) for this apparent habitat shift during ontogeny need to be investigated in future studies.
Feeding ecology
Individuals of T. marginatus from both habitats
consumed large amounts of kelp tissues (M. pyrifera or L. trabeculata), but they differed in the
proportion of other food items. High prevalence of
the habitat-forming algal species in stomachs has
also been observed for other majid species (Leighton 1966; Aracena 1971; Hines 1982; Woods 1993),
and for other species associated with kelp habitats,
such as echinoids, gastropods, and fishes (PerezMatus et al. 2012). Species that feed on habitatforming kelps obtain certain benefits, which include
a large biomass and a predictable availability of
resources (Leighton 1966; Wolcott & O′Connor
1992; Daly & Konar 2010; Hultgren & Stachowicz
2010).
Examination of the natural diet of T. marginatus
showed that in general it can be considered an herbivorous species, but that some individuals (especially adults) also include animal material in their
diet. Other majid crabs, such as Loxorhynchus
crispatus STIMPSON 1857, Pugettia richii DANA 1851,
Notomithrax ursus (HERBST 1788), Taliepus dentatus, and Eurynolambrus australis H. MILNE
EDWARDS & LUCAS 1841 also consumed some animal material together with the algae dominating
their diets (Hines 1982; Manriquez & Cancino
1991; Woods 1993; Woods & McLay 1996; Cumillaf 2010). Animal food may play a role as a critical
nutrient supplement (Wolcott & O′Connor 1992)
for growth and reproduction. Algal tissues are
poor sources of essential amino acids, vitamins,
and sterols, compared with animal material. Nitrogen is considered a limiting nutrient for herbivorous crabs (Wolcott & O′Connor 1992). For
instance, nitrogen assimilation efficiencies from an
141
algal diet may be 30% lower than those from an
animal diet (Wolcott & Wolcott 1984). Therefore,
a supplement of animal protein in the diet might
benefit growth and possibly also the reproductive
output of kelp crabs.
Our results showed differences in the diet of T.
marginatus with respect to crab size, similar to
results reported for many other crab species (Hines
1982; Stevens et al. 1982; Choy 1986; Woods 1993;
Woods & McLay 1996). In majid crabs, body size is
a limiting factor during resource utilization (Hines
1982). Different sizes at sexual maturity are also a
reflection of species-specific abilities to use microhabitats (e.g., crevices) as refuges from predators
(Hines 1982). In our study, the analysis of diet composition within each habitat suggested that immature crabs differ from adults in the use of the kelps.
As members of the genus Taliepus live on the stipes
and blades of large kelps (Santelices 1989), kelp
architecture may constrain their foraging behavior,
especially of juvenile and subadult individuals.
While there are extensive open spaces under the
arborescent L. trabeculata, the closely spaced blades
of M. pyrifera offer visual protection along the stipes all the way down to the holdfasts (Villegas et al.
2008), allowing crabs to move up and down within
the protective cover of the canopy. As the majority
of nonkelp food is found in the kelp holdfasts and
on the surrounding seafloor (Santelices 1989; Thiel
& Vasquez 2000; Ortiz 2008; Villegas et al. 2008),
it is likely that in M. pyrifera all crab sizes descend to the bottom to obtain these food items,
while the blade-less stipes of L. trabeculata restrict
the movement of juvenile and subadult crabs. This
interpretation is also supported by the fact that
small kelp crabs have a substantially smaller
activity range than adult crabs (Hultgren & Stachowicz 2010).
As kelp forest systems have high trophic complexity (e.g., multiple connections between a wide
diversity of consumers and resources), development
of adaptive foraging behaviors is important. Most
organisms exhibit specific feeding rhythms
(Hines 1982; Jesse 2001; Kronfeld-Schor & Dayan
2003; Hultgren & Stachowicz 2010). Despite the
differences in kelp forest structures, members of
T. marginatus showed a similar daily feeding cycle
in both kelp habitats, with a mostly nocturnal
feeding behavior. The tendency of T. marginatus to
feed more at night than during the day may also
help mitigate predation risks, very similar to
what has been suggested for other species of kelp
crabs (Aris et al. 1982; Hultgren & Stachowicz
2010).
Invertebrate Biology
vol. 132, no. 2, June 2013
142
Jofre, Ortiz, & Thiel
Fig. 6. Hypothetical model of the life cycle of kelp crabs Taliepus spp., highlighting the importance of different species
of macroalgae. Based on results from the present study and from Pardo et al. (2007) and Palma et al. (2011).
Conclusions and outlook
Kelp serves as both an important foundation species and a significant energy source for much of the
nearshore food web (Dayton 1985; Graham 2004),
both at the community and ecosystem level (Ortiz
2008, 2010). The present results on habitat use and
feeding behavior demonstrate that T. marginatus
uses the macroalgae as food and possibly as refuges
during most part of its benthic life cycle (Fig. 6).
The results confirm that T. marginatus is an omnivore in both types of kelp habitat, maintaining a
strong dependence on kelp tissues throughout their
lives, albeit adding other food items as they grow.
Both M. pyrifera and L. trabeculata are subject to
intensive exploitation (>70,000 tons in 2010) along
the Chilean coast (SERNAPESCA 2010). This has
led to a notable reduction in the density and coverage of kelp beds. In addition, the effects from El
Ni~
no Southern Oscillation (ENSO) also alter the
extent of kelp beds (Vega et al. 2005; Gaymer et al.
2010), even causing local kelp extinctions. Because
these kelp forests are habitats for the reproductively
active populations of T. marginatus, the continued
persistence of both kelps is likely to be important
for the population dynamics of this kelp consumer.
Acknowledgments. We thank Paula Ruz, Rosita Chavez, Manuel Rojo, Luis Rojas, Claudio Silva, Rodrigo
Saavedra, Leonardo Campos, and Carlos Alvarez
for
their help in the fieldwork. In particular, we are grateful
Invertebrate Biology
vol. 132, no. 2, June 2013
to several anonymous reviewers and to Lucas Eastman
for their constructive comments, which were of great help
in improving the manuscript. During the preparation of
this manuscript, David Jofre Madariaga was partially
supported by the CONICYT fellowship program (Becas
para Estudios de Magister). This study was financed by
FONDECYT 1040293.
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