Download Territoriality in the South African Intertidal Limpet Scutellastra

Territoriality in the South African Intertidal
Limpet Scutellastra longicosta
Amanda Heidt, Amrita Khalsa, Shannon Myers,
Travis Trinh, Victoria Wade
Abstract
The existence and effects of territoriality are documented in vertebrate systems but have received
less attention among invertebrate species. This study attempts to create a clear and concise
working definition of territoriality through the experimental confirmation of three tenets in the
South African Long-Spined Limpet Scutellastra longicosta, a species suspected of displaying
territoriality as a result of its mutualistic relationship with the brown alga Ralfsia verrucosa. We
posited three criteria for establishing territoriality: (1) uniform distribution, (2) restricted
movement to the immediate territorial space (garden), and (3) the presence of defensive behavior
(i.e. active expulsion of intruders). Spatial distribution was found to be uniform (p= 0.035) when
accounting for a correlation between limpet size and garden size (p= 0.0002). Movement was
restricted to a region well within the mean garden radius (p= 0.0001). Lastly, in situ
manipulations induced territorial and homing behaviors among territory holders and transplanted
individuals (p= 0.0001), respectively. The statistical confirmation of these tenets has
ramifications in standardizing the way territoriality is studied in the field. In addition, it provides
a baseline for examining the role of territoriality in maintaining the diversity and stability of
localized intertidal ecosystems.
Introduction
In community ecology, competition is thought to be one of the most important processes
driving the structure and function of natural species assemblages [22]. In particular, competition
for space has received a great amount of attention to better understand distribution and
abundance and species compositions in coastal marine ecosystems such as the rocky shore
[24]
. The sheer amount of theory to arise from studies undertaken along the world's coastlines,
exemplified in landmark papers such as Paine ‘66[24], Connell ‘77[6], and Sousa ‘79[31], lends
credence to a rich source of interactions between the physical environment and those organisms
contained therein. Equally as numerous are the strategies that have evolved to combat abiotic
factors such as desiccation and temperature fluctuations, as well as biotic interactions such as
resource competition and predation.
Novel strategies amongst individuals have evolved to maximize fitness in a system
largely dominated by limitations, either for space or for other resources. Traditionally, it can be
difficult to tease apart these biotic and abiotic effects, as a limitation on an abiotic factor such as
1 space can drive fierce competitive interactions between individuals [2-3]. One manifestation of
these interactions is the development of territoriality, a prevalent example of how best to secure
resources. A result of territorial behaviors, including competitive exclusion and territory
maintenance, is that some species significantly affect their environment in terms of localized
habitat modification and species composition. These interactions create a system of habitat and
species mosaics on both small and large geographic scales. In turn, habitat mosaics can support
a broader level of overall species diversity [9,14-15,18-19,25]. Territorial behaviors have been shown
in a variety of intertidal species, from blennoid fishes [10] to birds [5] to limpets [1-4,12-13,28,30,33,35].
Territoriality is a thread that links many limpets together, as several species demonstrate
some degree of territorial behavior, primarily Scutellastra longicosta, Scutellastra caerulea, and
Lottia gigantea [1-4,12,27-28,30,32]. The forms that these behaviors take are as variable as they are
effective. L. gigantea has been studied extensively and has been shown to defend a small
territory (< 900 cm2) while moving locally to forage [28]. Contrastingly, Scutellastra cochlear
maintains a territory of red algae not much larger than the size of its own body, taking many
years to mature and moving very little (if at all) during that time [2].
S. Longicosta is a species of South African limpet suspected of engaging in territoriality
as a byproduct of a mutualism with the brown algae Ralfsia verrucosa [8,11,21]. Characterized by
long protrusions extending outward from the shell, these spines grant the animal a two-fold
advantage: (1) they allow the animal to extend its surface area without a drastic increase in body
size, as the visceral mass extends into each spine, allowing for greater suction and (2) the spines
act as a tool for the animal to pry off intruders from its territory [2]. Past research has suggested
that mutualistic species affect algae via biotic and abiotic factors such as grazing and nutrient
supplementation by herbivores [20,32]. By grazing away existing algae, S. longicosta provides a
bare substratum required for settlement by Ralfsia. Once established, the limpets cultivate and
fertilize their space through feces and mucus [8], promoting growth. In addition, individuals will
directly engage any intruders, driving away any would-be competitors or algal predators. Both
juvenile and adult S. longicosta prefer to feed upon R. verrucosa, and through differentiation of
life cycles have minimized intraspecific competition for this resource [2,26].
These seemingly territorial behavioral patterns have been well-documented [1-4,12,2728,30,32]
, and it may be appealing to brand this an example of territoriality in action, but very little
work has been undertaken to develop a concrete working definition of what actually constitutes
2 territoriality. An analysis of the methodology used in studying vertebrate territoriality found that
only 12% of the papers actually provide an operational definition of the word, and that within
this group 50% used only the single criterion of 'defended area' as an indicator [16]. No such largescale analysis has yet been undertaken in establishing a working definition of territoriality in
invertebrates, although there would certainly be overlapping factors at play. A review of
ecological determinants of vertebrate territoriality determined food resources (and several related
variables such as quantity, predictability, distribution, etc.) to be the main ecological driver [17],
and the mutualistic relationship between S. longicosta and R. verrucosa seems to support this
idea.
The purpose of this paper is to take the first step in establishing concrete tenets of
territoriality, here defined as “the behavior of an organism in defining and defending its
territory.” Specifically, we would like to begin the discussion of how best to frame this
phenomenon in the context of an invertebrate species. We propose the following questions as
indicators of true territoriality: (1) Does S. longicosta exhibit uniform distribution, (2) Is
movement restricted to the immediate territorial space (garden), and (3) Do individuals exhibit
territorial behavior (i.e. active expulsion of intruders)? In establishing the existence of these
three tenets in a population of S. longicosta, we hope to provide a means for defining
territoriality in the field.
Materials and Methods
Site Description
This study was conducted in the Western Cape of South Africa, in the South-Western
Cape marine bioregion, near Betty’s Bay, approximately 0.5 km north of the Stony Point, and
just below Mooi Hawens resort (S: 34.37371, E: 018.88407). The shoreline at our site is largely
composed of bedrock and various aggregate ranging from large, jagged boulders to small pebbles
that together form a substantial and varied rocky intertidal region. Our study site is characterized
by smooth bedrock, an incline of less than 15 , minimal topographic variance, extensive R.
o
verrucosa cover, moderate to high densities of adult S. longicosta, and a tidal range of 50-85 cm
above the mean lower low water (MLLW). On the rocks and in the various pools surrounding
our study site, there is a plethora of other invertebrate, algal species, birds, and fish. Our site is
3 situated in the lower-mid tidal range. Due to seaward reef-like subtidal and exposed rock
formations, wave exposure is minimal and the sites experience only gentle tidal flushing each
day.
General Methods
We tested our general hypothesis that S. longicosta exhibit territoriality by performing
two observational studies and one manipulation study in order to test the following three specific
hypotheses: individuals are uniformly distributed (distribution), largely remain within home
territories (movement), and exhibit some form of defensive and or homing behavior (behavior).
Studies were conducted during the month of April 2013, in Betty’s Bay, South Africa at our site,
described previously. This site satisfies conditions where S. longicosta have been observed in
highest densities.
We initially investigated the correlation between several parameters of limpet size and
garden area and later applied it to both our distribution and movement studies. We randomly
removed 15 individuals of varying sizes from the substrate (using a knife to pry them from the
surface) and took the following measurements: length of the largest diameter (spine-to-spine),
height, and weight. Additionally, we measured between the farthest points of each garden to
estimate the diameter (and thereby determine the area), and used statistical analysis to find the
best variable to use for determining the area of an individual’s corresponding garden. (We
performed a linear regression on each possible parameter versus garden area and chose the most
significant one.) All statistical analyses were performed using a 95% confidence level.
Distribution
In order to test the hypothesis that S. longicosta exhibit uniform distribution, we sampled
quadrats in areas meeting our substrate criteria and statistically compared the observed
distribution of S. longicosta to the two other possible distributions, random and clumped, to
either support or reject our expectation of uniformity under the first tenet of territoriality.
Quadrats were constructed using 1.5 inch PVC pipe that measured 25 x 25 cm. We
sampled our entire site by laying a quadrat down at one boundary (defined by where substrate no
longer met our criteria) and rolling it over in all directions until the entire site had been sampled.
For each quadrat placed, we recorded the number of S. longicosta individuals with at least half of
4 their shells contained within the quadrat.
Distribution was assessed by analyzing the variance to mean ratio (V:M) of the number
of S. longicosta individuals across all quadrats and comparing the calculated value to known
V:M values associated with either random (V:M = 1), clumped (V:M > 1), or uniform
distributions (V:M < 1). Additionally, we conducted a Kolmogorov-Smirnov (KS) test in order
to compare the obtained distribution data to that of a Poisson (random) distribution.
Although not directly utilized in our testing of the above hypothesis, for a visual
representation of distribution, we manually laid out an XY plot using seamstress tape. We
measured the X and Y positions and greatest length for each individual in the plot and calculated
their garden area using the formula derived from the previously mentioned correlation. We
generated a bubble plot to represent the territory size and respective location for each individual.
Movement
In order to test the hypothesis that S. longicosta exhibit limited movement outside their
home territories, we monitored individuals’ daily movement in our study site. We compared
calculated territory size for each individual to observed movement and determined if S.
longicosta’s mean movement extended beyond home territories.
We randomly tagged and measured 109 individuals at greatest spine-to-spine diameter.
We tagged individuals using super glue to attach 3x5 mm rigid, plastic tags at just below the
apex of individuals’ shells. We placed corresponding substrate tags directly adjacent to each
individual. We marked all tagged individuals with a dot of nail polish as a means to monitor our
tag failure rate. Immediately following tagging, we measured each individual from center of
shell tag to center of substrate tag for seven consecutive days at low tide.
We calculated mean movement across all individuals and compared it to mean radius (as
a proxy for territory), derived from the established correlation of shell length to garden size
previously mentioned, using a two-sample, one-tailed t-test. We interpreted the results of the test
assuming a null hypothesis of movement greater than or equal to mean garden radius.
Behavior
In order to test the hypothesis that S. longicosta exhibit defensive/homing behavior, we
manipulated the spatial positioning of individuals in relation to both conspecifics and to their
5 home territories. If S. longicosta defend their home territories, then placing conspecific
competitors in close proximity to other individuals’ home territories should create a defensive
response in residents that will generate a measurably different response by intruders when
compared to those placed in vacant territories. Homing behavior was determined by comparing
movement between individuals moved to either vacant or occupied territories.
We conducted manipulations at the same site used in the previous movement study so as
to utilize previously tagged individuals whenever possible. For each trial we used sets of five
similarly sized adult individuals residing in close proximity to each other. We located ten such
trial groups and tagged any individuals not previously tagged. For each trial, we removed
individual 1 and placed it in its original location to serve as a control for the effect of removing
individuals from their substrate. We
removed individual 2 and discarded it to
create a vacant garden. We removed
individual 3 and placed it on the scar of
individual 2. We removed individual 4 and
placed it directly adjacent to
unmanipulated individual 5 on its home
scar. We conducted a total of ten sets of
manipulations.
We took measurements from the
center of shell tag to the center of substrate
tag for individuals 1,3,4, and 5 in each trial group immediately following manipulation, and then
again each day at low tide for seven consecutive days. We compared mean movement of
individuals 1,3, and 4 across all trials and replicates using an ANOVA test.
We expected one of three possible outcomes as the primary driver of movement: if only
transplants moved to occupied territories move, we will conclude defensive behavior is
responsible; if transplants moved to both occupied and empty territories move equally, we will
conclude homing is responsible; if transplants moved to occupied territories move more than
transplants moved to empty territories, we will conclude both defensive behavior and homing is
responsible.
6 Results
After we performed linear regressions on each of the potential parameters of size to
garden area, we found length to be the most significant (P < 0.0002) (Figure 2). We used the
following formula to calculate garden area: Area of garden = -91.72303 + 29.321444*Length +
5.5994887*(Length-4.594)^2.
Distribution
The results of the experiment
designed to test for uniform distribution of
S. longicosta strongly support the
hypothesis that S. longicosta are uniformly
distributed based on the variance to mean
ratio being less than one (0.632) and the
distribution being different from Poisson
distribution (P=0.035) (Figure 3). A total
of 80-90% of all quadrats contained
between one and two limpets (Figure 4).
7 Movement
The results of the experiment designed to test if S. longicosta move farther than the radius
of their garden strongly support the hypothesis that S. longicosta limit their movement to within
their garden (P<0.0001) (Figure 5). Average movement = 0.67 cm and average garden radius =
3.97 cm.
Defensive Behavior
The results of the experiment
designed to test for defensive behavior
strongly supports the hypothesis that S.
longicosta defend their territories. When
placed in a territory with an existing resident,
on average the transplant would move more
than when placed into an empty territory (P
= <0.0001) (Figure 6). On average the
control moved 1.24cm, the transplants
moved into an empty territory moved
12.65cm, and the transplants moved into
occupied territories moved 32.63cm.
Discussion
Based on the results, we were able to
confirm each of the 3 tenets, and in doing so
suggest the presence of territoriality in the
limpet species S. longicosta. Territoriality
has a variety of implications for the health
and maintenance of ecological
systems. While many vertebrate studies
focus on relatively large territories and even
larger home ranges, such models used to
examine territories and territorial
8 interactions are limited by the logistics of working on such large scales. Under a finer lens of
analysis, small invertebrate species such as S. longicosta can have drastic localized effects in
altering the landscape and helping to impose strict distributional regimes. More broadly, this is a
species that also paradoxically may help maintain higher levels of diversity through continued
disturbance [22] and in so doing be responsible for increasing system stability [24].
Distribution
Individuals adhered to a uniform distribution (Figure 3) consistent with relatively equally
spaced, non-overlapping gardens. When interpreting these results, it is important to bear in mind
a positive correlation between limpet size and garden size (p = 0.0002, Figure 2), as a spatial
representation (Figure 4) may appear random at first glance. However, we were able to
statistically factor out both random and clumped distributions using a variance: mean ratio
(0.632, Figure 3). Furthermore, we were able to show statistical deviations from Poisson using a
KS Test (p = 0.035, Figure 3), giving additional statistical power to our final results. A uniform
distribution allows for individuals to exist in close proximity without actually coming into
contact, maximizing resources that may be patchily distributed in areas of varying density.
Movement
Movement was shown to be minimal (Figure 5), as would be anticipated in a species
initially described by Branch as “non-migrating [2].” Limpets were expected to move no further
than the edges of their garden (as measured by the radius), and this was shown to be true across
the duration of the study (p = 0.0001, Figure 5). The average total movement (0.67 cm) was
significantly less than the average garden radius (3.97 cm), indicating very little motion (Figure
5). This lack of movement is most likely the result of a need to protect the garden space from
any potential intruders. Excluding the need to graze and fertilize Ralfsia, energy is best stored
for use in territory defense.
Behavior
Manipulations performed in situ (Figure 1) as a means of assessing territoriality yielded a
two-fold response: not only was territoriality an inducible phenomenon when intruders were
introduced, but individuals that were moved into territories (occupied or not) were shown to
9 demonstrate homing (Figure 6), a concept not initially addressed in the experimental
design. When placed in a territory with an existing resident, movement by the transplant was
greater on average (32.63 cm) than when placed into an empty territory (12.65cm), indicative of
a response to territorial behavior (p= 0.0001, Figure 6). Controls moved very little (1.24cm,
Figure 6), behavior supported by movement data (Figure 5).
Territoriality has applicability in several ecological paradigms. The idea of intermediate
disturbance was first described by Connell [7] and posited that intermediate levels of disturbance
in a system would promote the highest levels of diversity. An analogous example would be the
way fire carves a terrestrial biome into patchy mosaics of territories in various stages of
succession [23]. Part of the mutualistic relationship between S. longicosta and R. verrucosa
involves the clearing of space for R. verrucosa to settle in higher densities than would be
expected in the absence of territoriality on the part of the limpet [2]. This relationship adds to the
mosaic of the local environment, promoting healthy levels of disturbance as well as increased
diversity. As an example, grazing by limpets has been shown to inhibit growth of Ulva spp., a
standard early successional species [6,21]. Indeed, unpublished algal species counts in this study
yielded no less than a dozen different species within the study space.
These other species, which contained members of all three algal divisions, took hold in
the proverbial “no man’s land” between limpet territories where no active grazing was
occurring. Gardens rarely overlap (Figure 4), and a uniform distribution averaging only 1-2
limpets per quadrat (Figure 3) means that oftentimes spaces exist between gardens that are
available for colonization by other algal species but too small for S. longicosta to establish
territories. Despite being outside of a defended territory, the aggressive behavior exhibited by S.
longicosta discourages other individuals (both co- and conspecific) from entering the area[2],
lowering grazing pressure.
While it seems paradoxical to suggest that S. longicosta promotes greater diversity while
simultaneously stimulating the growth of a single algal species and excluding other species from
the area, it is again a matter of scale. On the smallest scales, S. longicosta does indeed surround
itself with only R. verrucosa. However, if overall diversity of algal species occurs as a result of
territoriality, on a larger scale vast configuration of S. longicosta occurring all along the South
African coast may contribute to a more healthy and diverse system. Suggestions of increasing
diversity leading to a more stable system have been championed by famous ecologists [9,14-15,18-
10 19,25]
for decades, and it may well be the case that concrete forces such as territoriality operating
in such a dynamic, space-limited system as the intertidal are essential for healthy ecosystem
functioning.
Diversity exists beyond the species of algae, but also in the limpets themselves. South
Africa supports at least two-dozen limpet species [26], and many co-occur in the same areas. As
mentioned previously, the life history strategies are as varied as the species themselves. S.
longicosta was shown to be largely static in its movement patterns (Figure 5) and has been
previously classified as a territorial, non-migratory species [2]. However, other species have
adopted extensive ranges of motion, nocturnal foraging behaviors, or strict substrate
requirements as a means of co-existing [1-4,34]. In turn, many predators have evolved to specialize
in limpet predation. For example, African Black Oystercatchers (Haematopus moquini) have
been described as specialized feeders of S. longicosta [26].
Homing was an unanticipated behavior that manifested itself within the manipulation
data (Figure 4). While not included in the tenets, homing is a behavior highly congruent with
territoriality and has been previously described in other members of Scutellastra [2, 29, 34]. In both
manipulations where a limpet was moved into a new territory (either with or without a territory
holder in place), individuals were observed moving back to their home scars, sometimes within
the scope of a single day. While some work has suggested a mucus trail as the mechanism by
which limpets return to home scars [8], this could not have been the case in this study as
individuals were pried off and moved without laying down a scent trail. How individuals were
able to return is undetermined, but it may well have been an unintended result of manipulation
design that allowed some individuals to be close enough after manipulation to pick up on cues
from the garden itself.
There were a few additional points of contention in our protocol we would like to address
in the hopes of guiding future research. To begin, we suggest a more thorough distributional
analysis of S. longicosta along the coast of Southern Africa, including any potential affinities for
certain topographical and substrate features or biological attributes such as the local algae
community. While certain general patterns in distribution exist [1], our field site presented a bit
of an anomaly across a relatively small spatial area. Though resolution was high enough to
achieve the desired statistical significance, bolstering the sample size would serve to lend
additional credence to our conclusions.
11 In addition, our study was constrained to periods of low tide when limpets were
exposed. The premise was that because limpets typically do not move out of water, any
manipulations and subsequent responses would not take place until the area was again
submerged. However, similar attempts by Branch [2] to prompt aggressive behavior failed to do
so in 35 out of 38 manipulations when performed out of water. This fact did not appear to
hamper our findings, as we found significant results and had a tagging failure rate of only 1%.
Though, it might prove more effective when dealing with greater sample sizes.
Having addressed these points, future work could take many potential
manifestations. Because S. longicosta is not as well studied as other territorial limpet species
(e.g. Lottia sp.), any forthcoming information is likely to prove insightful. While it is known that
they are broadcast spawners [1,26], less is known about age-based population structure, including
how juveniles factor into the territorial scheme. Smaller individuals were observed with
corresponding smaller territories, but as of yet very little information exists to describe the cues
individuals use in the transition to establishing territories of their own.
Furthermore, given the seemingly intensive intraspecific [2], competition taking place as a
result of territoriality, a logical progression would be to test for the presence of interspecific
competition between other intertidal species, in congruence with work done by Branch [3]. An
example interaction founded on field observations occurs between S. longicosta and another nonmigrating species of limpet, Cymbula oculus. While C. oculus does not actively maintain a
territory [34], it was found living in close proximity to S. longicosta, and in several cases was
close enough to elicit a potential response. Shifting the focus from intra- to interspecific
competitive forces may yield additional insight into the ways in which S. longicosta helps shape
local community structure.
Ideally, this study would serve as a baseline from which to launch further
enquiry. Additional time, intensive surveying, and a larger working sample size would help to
standardize and cement the ideas presented herein. However, the first step of clearly defining
three tenets and proving that they have applicability in the field is important if only for its
novelty. It is our hope that this discussion on territoriality, especially within the context of the
relatively understudied invertebrates, can be carried forward.
12 References
1. Branch G. M. 1971. The ecology of Patella Linnaeus from the Cape Peninsula, South Africa. I. Zonation,
movements, and feeding. Zoologica Africana 6: 1-38.
2. Branch G. M. 1975. Mechanisms reducing intraspecific competition in Patella Spp.: migration, differentiation
and territorial behaviour. Journal of Animal Ecology. 44: 575-600.
3. Branch G. M. 1976. Interspecific competition experienced by South African Patella species. Journal of
Animal Ecology 45: 507-529.
4. Branch G. M. 1981. The biology of limpets: physical factors, energy flow, and ecological interactions.
Oceanography and Marine Biology Annual Review 19: 235-380.
5. Colwell, M. A., and R. L. Mathis. 2001. Seasonal variation in territory occupancy of non-breeding Long-billed
Curlews in intertidal habitats. Waterbirds 24: 208-216.
6. Connell, J. H., and R. O. Slatyer. 1977. Mechanisms of succession in natural communities and their role in
community stability and organization. American Naturalist 111: 1119-1144.
7. Connell, J. H. 1978. Diversity in tropical rain forests and coral reefs. Science 199: 1302–1310.
8. Connor, V. M., and J. F. Quinn. 1984. Stimulation of food species growth by limpet mucus.
Science 225: 843-844.
9. Elton, C. S. 1958. The ecology of invasions by animals and plants. Methuen, London.
10. Goncalves, E. J., and V. C. Almada. 1998. A comparative study of territoriality in intertidal and subtidal
blennioids (Teleostei, Blennioidei). Environmental Biology of Fishes 51: 257-264.
11. Kaehler, S., and P. W. Froneman. 1999. Temporal variability in the effects of grazing by the territorial limpet
patella longicosta on the productivity of the crustose alga Ralfsia verrucosa. South African Journal of
Science 95: 121-122.
12. Keasar T. and U. N. Safriel. 1994. The establishment of a territory: effects of food and competitors on movement
patterns in Patella caerulea limpets. Ethology Ecology & Evolution 6: 103-115.
13. Lasiak, T. 2005. Spatial variation in density and biomass of patellid limpets inside and outside a marine
protected area. Journal of Molluscan Studies 72: 137-142.
13 14. Lehman, C. L., and D. Tilman. 2000. Biodiversity, stability, and productivity in competitive
communities.American Naturalist 156: 534-552.
15. Macarthur, R. 1955. Fluctuations of animal populations, and a measure of community stability. Ecology
36: 533-536.
16. Maher, C. R., and D. F. Lott. 1995. Definitions of territoriality used in the study of variation in vertebrate
spacing systems. Animal Behaviour 49: 1581-1597.
17. Maher, C. R., and D. F. Lott. 2000. A review of ecological determinants of territoriality within vertebrate
species. American Midland Naturalist 143: 1-29.
18. Margalef, R. 1969. Diversity and stability: a practical proposal and a model of interdependence. Pages 25–37 in
Diversity and stability in ecological systems. Brookhaven Symposium in Biology 22. Brookhaven National
Laboratory, Upton, N.Y.
19. May, R. M. 1972. Stability and complexity in model ecosystems. Princeton University Press,
Princeton, N.J.
20. McCormick, P. V., and R. J. Stevenson. 1991.Grazer control of nutrient availability in the periphyton.
Oecologia 86: 287-291.
21. McQuaid, C. D., and P. W. Froneman. 1993. Mutualism between the territorial intertidal limpet Patella
longicosta and the crustose alga Ralfsia verrucosa. Oecologia 96: 128-133.
22. Menge, B. A., and J. P. Sutherland. 1987. Community regulation - variation in disturbance, competition, and
predation in relation to environmental-stress and recruitment. American Naturalist 130: 730-757.
23. Minnich, R. A. 1983. Fire mosaics in southern-California and northern Baja California. Science 219: 1287-1294.
24. Paine, R. T. 1966. Food web complexity and species diversity. American Naturalist 100: 65-&.
25. Odum, E. P. 1959. Fundamentals of ecology. 2d ed. Saunders, Philadelphia.
26. Peschak, Thomas. 2005. Currents of contrast: life in Southern Africa's two oceans. Struik Publishers (July
14, 2006).
27. Plaganyi, E. E. and G. M. Branch. 2000. Does the limpet Patella cochlear fertilize its own algal garden? Marine
Ecology Progress Series 194: 113-122.
28. Schroeder, S.L. 2011. The behavioral ecology and territoriality of the owl limpet, Lottia gigantea (Doctoral
dissertation).
14 29. Sebastian, C. R., C. N. Steffani, and G. M. Branch. 2002. Homing and movement patterns of a South African
limpet Scutellastra argenvillei in an area invaded by an alien mussel Mytilus galloprovincialis. Marine
Ecology Progress Series 243: 111-122.
30. Shanks, A. L. 2002. Previous agonistic experience determines both foraging behavior and territoriality in the
limpet Lottia gigantea (Sowerby). Behavioral Ecology 13: 467-471.
31. Sousa, W. P. 1979. Disturbance in marine inter-tidal boulder fields - the non-equilibrium maintenance of
species-diversity. Ecology 60: 1225-1239.
32. Sterner R. W. 1986. Herbivores' direct and indirect effects on algal populations. Science 231: 605-606.
33. Wright, W. G. 1982. Ritualized behavior in a territorial limpet. Journal of Experimental Marine
Biology and Ecology 60: 245-251.
34. Underwood A. J. 1979. The ecology of intertidal gastropods. Advances in Marine Biology 16: 111-210.
35. Wright, W. G., and A. L. Shanks. 1993. Previous experience determines territorial behavior in an
archaeogastropod limpet. Journal of Experimental Marine Biology and Ecology 166: 217-229.
15