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AQUATIC CONSERVATION: MARINE AND FRESHWATER ECOSYSTEMS

Acuatic Conserv: Mar. Freshw.Ecosyst. 11: 19-30 (2001)

COMMUNITY PATTERNS GENERATED BY HUMAN HARVESTING ON

CHILEAN SHORES: A REVIEW

Carlos A. Moreno
Instituto de Ecología y Evolución
Universidad Austral de Chile
Casilla 567, Valdivia

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ABSTRACT

1. The Chilean rocky coast has been exploited for food by coastal gatherers for at least 8500
years BP and probably was an important factor in how prehistoric people were able to
colonize the South Americas Pacific Rim. The main species targeted in the past were the
same as those today except that now the gatherers are resident and the fishing activity is
more intense and persistent.
2. With many pertinent studies from around the world having been published on this topic,
mostly conducted in Marine Reserves, this review tries to identify the main patterns that can
help us recognize, in the Chilean intertidal, the degree of exploitation on wave exposed and
wave protected rocky shore habitats.
3. Three clear patterns were identified depending on the trophic level adopted by the human
gatherers in the food chain of the intertidal zone. First when the humans act as herbivores,
collecting the large laminarian Durvillaea antarctica, adult plants disappear from the
accessible sites, especially the midlittoral, semi-exposed and exposed habitats.
4. Second, when humans harvest the ecologically important herbivorous archeogastropoda
Fissurella spp., this results in the red alga Mazzaella laminarioides covering almost 100%
of the midlittoral rocks. Third, when humans become top predators by collecting the
muricid carnivore Concholepas concholepas, then bivalves, mainly Perumytilus
purpuratus, cover the rocks in multiple layers.
5. These patterns contribute to the evaluation of the state of conservation of the Chilean
rocky intertidal shores, especially because the north and the south are beginning to be
connected by a new coastal road. Thus it is necessary to evaluate urgently, on a large spatial
scale, the state of conservation of these communities, in order to help select the appropriate
places for establishing Marine Reserves.

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INTRODUCTION

The increase in the human population has resulted in an increase in the utilization of
natural resources with subsequent effects on ecosystems. In terrestrial systems, human
interference and its effects on the distribution and abundance of animal and plant
populations has been long recognized (Brown and Gibson, 1983 and cited references;
Moore, 1985). However, in marine intertidal communities the study of the effects of human
interference has only just begun in the last two decades (Moreno et al., 1984). Previously,
human activities such as the discharge of waste and contaminants were considered the only
relevant factors in the deterioration of natural marine assemblages. However, when humans
selectively collect organisms for consumption or ornamental purposes, they too act as
predators directly affecting community structure and organization.
The use of protected marine zones or marine reserves has been the major tool to help
understand human induced perturbations of ecological processes and the effects on natural
populations and communities. Recent reviews (Rowley, 1994; Guénette et al., 1998) have
described the application of such ecological knowledge in fisheries management whilst
Castilla (1999) considers the challenges of undertaking basic ecological research that can’t
be conducted today without considering the consequences of human impact.
In the last 50 years manipulative experiments have contributed much to our
understanding of local patterns of diversity, distribution and abundance of intertidal
organisms on rocky shores. Some of the key concerning dynamics of local rocky intertidal
communities were, 1) the recognition that competition between populations of benthic
organisms that use space can be regulated by predation in the rocky intertidals. This process
can help to understand the space distribution (e.g. zonation) and abundance of sessile
invertebrates and algae (Connell, 1961, 1972; Paine, 1966; Lubchenco, 1978), 2) the
finding that physical perturbations can exert the same type of effects over the competitors
and the effect of mortality along ecological succession (Sousa, 1979), 3) the incorporation
of recruitment as a factor that affect community structure (Underwood and Denley, 1984).
All these ecological processes were related in comprehensive models of community

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organization by Menge and Sutherland (1976, 1987), reviewed by Sih et al. (1985) and
sintetized by Raffaelli and Hawkins (1996).
In this review our main interest is to analyze the effects that human activities have
on the processes that regulate the distribution and abundance of organisms on rocky
intertidal and its related subtidal habitats in order to identify patterns of human perturbation.
This because we need identify the criteria of “Naturalness” (sensu Salm & Price, 1995) as
part of a program for found the sites along the central-south coast of Chile for stablished
marine protected areas. This is not a simple task since most of the quantitative indices of
community structure (species richness, Shannon-Weaver, dominance, etc.) cannot be
related to human impact, because few studies show a positive or negative effect on these
variables. Even with clearly different community structures the numbers could be the same
(Keough and Quinn, 1991). Similar restrictions apply to the multivariate analysis because
they need to be used in conjunction with an experimental approach to the analyses of causal
links (James and McCulloch, 1990). Unfortunately, for studies of large spatial scale, it is
necessary to use a quantitatives descriptive approach and its results can be better understood
if we can identify those patterns generated by human perturbations obtained in experimental
research. In such way that the trends shown by multivariate statistical analyses can be
interpreted under an ecological dynamic scope. The increasing interest of the scientific
community in marine conservation in Chile and especially along the coast of the
Southeastern Pacific region, make it important to establish those patterns of perturbations
generated by humans when they harvest species from the intertidal rocky shores.

HISTORIC RECORDS OF HUMAN EXPLOITATION OF MARINE SYSTEMS

The first signs of human exploitation of marine resources come from shell middens
left by prehistoric societies and studied by archaeologists (Avery & Siegfried, 1980;
Shiappacasse and Niemeyer, 1964; Montane, 1964; Speed, 1969; Parkington, 1977;
Dillehay, 1984). Stratigraphic evidence suggests that human colonization has produced
important changes in the local biota in the Polynesian islands (Kirch, 1983) and in Scotland
(Andrews et al., 1985). The best case comes from the Aleuts (Simenstad et al., 1978).
Aleuts and pre-aleuts over-exploited the populations of sea otters moving to other islands as
numbers declined. Stratigraphic analyses show a negative relationship between sea otters

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and limpets and urchins. The reappearance of sea otters was associated with increases in the
abundance of coastal fish and kelp beds.
On Chilean intertidal shores Jerardino et al. (1992) have shown that the molluscan
species initially exploited 8500 BP are almost the same as those exploited at present by
shellfish gatherers in central Chile. Jerardino et al. (1992) suggest it is likely that the pre-
Columbian people may have temporarily or permanently modified sectors of the rocky
intertidal at Punta Curaumilla, and they also make references at other sites in Chile with
similar middens associated with human activity.

EFFECTS OF HUMAN PREDATORS ON POPULATIONS

Humans are size-selective predators choosing larger individuals. Branch (1975) pointed out
that human consumption reduced the maximum size of the intertidal limpet Helcion
concolor in South Africa. This has important consequences for the limpet populations:
Firstly, a decrease in maximum length will dramatically reduce the biomass. Thus, it will
be necessary to collect more animals for equivalent amounts of meat.
Secondly, a reduction in body size reduces gonad output with a decrease in fecundity of the
population.

Short term studies.

Most of the evidence for the effect of human predation on the population structure
of marine invertebrates comes from comparisons between areas exposed to humans versus
reserves. Siegfried et al. (1985), Hockey and Bosman (1986) and Hockey et al. (1988)
demonstrated that in the South African region of Transkei, human predation reduced the
mean size of populations of mussels (Perna perna), limpets (Sentellastra granularis and
Cellana capensis) and oysters (Crassostrea cuccullata). Similar results were found for
Central and Southern Chile for gastropods (Concholepas concholepas) and limpets
(Fissurella spp.) (Moreno et al., 1984; Castilla and Duran, 1985; Moreno et al., 1986; Oliva
and Castilla, 1986; Duran et al., 1987) and on the Pacific coast of Costa Rica for pulmonate
limpets (Siphonaria gigas) (Ortega, 1987). In contrast, Castilla and Fernández (1998) did

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not find any significant effect in the size of crabs between protected and exploited
populations at Central Chile.
In general, humans take a wide range of species from intertidal shores. However,
they prefer some of the species and their larger size classes. Siegfried et al. (1985) noted
that humans lose interest in smaller prey, switching to alternate prey items. For example, in
Transkei, P. perna accounted for 92% of all animals collected in 1978. The corresponding
proportion was 57% in 1984. In contrast, the proportion of limpets increased from 7% in
1978 to 37% in 1984. The difference in size structure of marine populations inside
versus outside reserves coincides with the presence and absence of human harvesting. This
could be attributed to differences in growth rate or intrinsic fluctuations in population
density (Seed, 1976). However, Ortega (1987) found no differences in growth rate of
limpets in areas accessible to humans and at a national park on the Central Pacific coast of
Costa Rica, but found substantial differences in mean size. Because growth rate can be
affected by environmental conditions and is often density dependent (Newell, 1979) it
should be measured when comparing exploited versus protected populations.
A slightly different approach to study the effect of human predation on populations
was taken by Moreno et al. (1984, 1986; see also Branch and Moreno, 1994). These
authors followed the response of populations of the limpet Fissurella picta after the
establishment of a Marine Reserve. They noted an increase in mean size of F. picta when
protected from humans. A similar response was observed for the gastropod Concholepas
concholepas (Moreno et al., 1986). In this case the establishment of large C. concholepas
in the intertidal zone indicated that this species was not physiologically prevented from
living there, as was previously thought.
Supplementary evidence that provides information on selectivity of large sizes of
prey by humans comes from inspection of shell middens accumulated after human
consumption and direct inspection of material collected by people (Hockey and Bosman,
1986; Ortega, 1987). However, at least two problems can influence this type of information:
one is the effect of accumulation of shells by physical environmental factors (Newton et al.
1993) and the second one, is the selection of the individuals made by the gatherers that,
before carryng home the larger shells, discard the smaller ones (Lasiak and Dye, 1989).
Humans also collect marine invertebrates for ornamental purposes. Zedler (1978) analyzed

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the effects of visitants on intertidal populations of the limpets Lottia gigantea and Lottia
digitalis in the Cabrillo National Park in California (USA) versus areas outside the park.
The human effect on limpet populations was basically the same as observed above. Thus,
humans have the same effect on populations regardless of the purpose of their collecting,
and this could be clearly recognized as a pattern when comparing exploited and non-
exploited intertidal shores.
Prey of invertebrate predators can exhibit an escape in size beyond which they
cannot be eaten (Paine, 1976). In contrast, there is no escape for large-sized prey items
eaten by humans: in this case the escape is for smaller individuals. Fast growth for
invertebrates preferred by humans will lead to higher mortality when they enter the larger
size classes. These prey may escape from other predators in spatial refuges. Humans are
not physiologically limited with respect to the capture of large prey items. Visual
predation and the use of tools and different techniques allow them to capture prey more
efficiently.
Human predation not only acts on individual sizes but also on population density.
This is probably the most important effect when considering predator-prey interactions.
Moreno et al. (1984) demonstrated that the density of F. picta tripled after two years of
protection in the Marine Reserve of Mehuin in Southern Chile, but this increase in density
in the long term, showed changes in abundance around the carrying capacity of the
environment, probably related with density dependent effects (Duarte et al. 1996).
The effect of human predation on population density of species will vary depending
on the accessibility of the habitat to humans. For example, Oliva and Castilla (1986) noted
that after two years of human exclusion the most dramatic changes in population density of
limpets occurred in habitats previously most accessible to people. Thus, limpets on
sheltered platforms showed greater changes in populations than those on wave exposed
platforms and vertical walls. Duran et al. (1987) and Siegfried et al. (1985) indicated that
human predators have different effects on prey populations depending on their density and
activity patterns, for instance during summer more people arrive to the coastal zone and
gather more organisms from the rocks. In winter for other side, the adverse meteorological
conditions reduce the impact.

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Long term studies.

Moreno and Rubilar (1997) indicated that for the Chilean intertidal communities a
time period up to ten years could be enough to encompass or exceed the generational time
of most of the species thus fullfilling one of the criteria stipulated by Connell and Sousa
(1993) for determining stability on the community, i.e. that observations of the community
be integrated at least to the next generation. Few studies have been published with this kind
of long-term time series for intertidal communities protected from human harvesting.
Duarte et al. (1996) present a long-lasting monitoring programme of the Fissurella
population at the Marine Reserve in Mehuin (MRM ; Valdivia, Chile). Changes in density
and distribution of keyhole limpets were detected during the first five years as a
consequence of human gatherer exclusion. But for the next 6 years a species habitat
segregation of the key-hole limpets occurred in the Marine Reserve and a dramatic fall in
the densities was detected, while the size structure comprised large, old individuals.
Competition for food, predation and problems with recruitment, are all possible
explanations for such changes in Fissurella picta and Fissurella limbata populations.
In this same Marine Reserve, Moreno (1995) and Moreno and Rubilar (1997)
studied the demographic processes affecting intertidal populations of the mussel
Choromytilus chorus over a 10-year period. In this study, they showed that the rise and fall
of this population was related to different processes that started with the ENSO (El Niño
Southern Oscillation) phenomenon of 1983, which led to the removal of large proportions
of sand by increased wave action and the growth of the red alga Gymnogrongus furcellatus.
This alga provides settlement habitat for the mussel thus enhancing recruitment. Davis and
Moreno (1995) demonstrated that habitat selection during settlement occurs in spite of
chemical deterrents in the alga against the mussel spat. During the period in which the
juveniles live attached to the alga they are protected from benthic predators (Moreno,
1995), although population numbers began to decline due to intraspecific competition (Seed
and Suchaneck, 1992), predation (Moreno, 1995) and mortality due to seasonal changes of
the sand level (Moreno, 1993). Finally, the mussels that have established on the rocky
bottom begin to be heavily predated by the size-selective, black oystercatcher, Haematopus
ater, which eats the same sizes of mussels as those harvested by humans at non- protected
habitats (Moreno, 1993; Moreno and Rubilar, 1997), illustrating both direct and indirect

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effects, and cascades in the food web. The oystercatcher and humans are competitors, both
affect the abundance of their filter feeding prey, but the humans outcompete the birds. A
similar competitive relationship to that described above for southern Chile has been
suggested as the cause of the extinction of the Canarian black oystercatcher (Hockey,
1987).
A totally different type of effect has been found by Castilla and Bustamante (1989)
and Bustamante and Castilla (1990) and is related with the spillover of algal propagules that
result in recolonization across Reserve borders. This, however remains one of the few
studies of such spillover (see Rowley, 1994). In Central Chile the brown alga Durvillaea
antarctica is exploited for human consumption. In the Las Cruces Marine Reserve it has
increased and this has led to greater recruitment outside this protected site. At the same time
the spatial distribution within the Marine Reserve began to change from the low intertidal to
the midlittoral. The same change was observed at exposed points in the Marine Reserve of
Mehuin, 850 Km south of Las Cruces Marine Reserve. This “new” vertical distribution can
also be observed at isolated sites in the Chilean southern archipelago zone. Other changes in
vertical distribution have been observed in Mazzaella laminarioides at Mehuin, even
although it is palatable to limpets (Moreno and Jaramillo, 1983). The same relationship was
recorded in other sites on the coast of Valdivia (Parra et al., 1992).
Based on this evidence, it appears that while the sizes of the invertebrate individuals
remain large in protected areas, density falls over time and the distribution changes,
probably due to density-dependent processes. This makes it necessary for other
complementary management measures in Reserves to be implemented (also see Allison et
al., 1998). Some algal species also changed their vertical distribution in the intertidal zone
at the same time that the herbivores changed, with palatable species decreasing their vertical
distribution and the non-palatable algae increasing their distribution. The best examples are
those of, Durvillaea antarctica on exposed shores and Mazzaella laminarioides in protected
habitats in Marine Reserves.

EFFECTS OF HUMAN PREDATORS ON INTERTIDAL COMMUNITIES

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Different patterns related to community structure and organization and the role that
humans play as part of the marine communities, including direct (i.e. between trophic
levels) and indirect (i.e. within trophic levels) effects of human predators can be described.

Direct effects of human predators

Hockey and Bosman (1986) showed that in Transkei relative abundances of algae
and sessile, inedible invertebrates were greater, and modal and mean sizes of exploited
species were smaller at exploited sites compared with protected sites. Thus, disturbance
through selective predation increased species richness.
Human exclusion in marine reserves has been shown to affect trophic chains
(cascade effects) that influence patterns of relative abundance, dominance and zonation on
rocky intertidal shores. In Mehuin, Southern Chile, the midlittoral zone of rocky shores was
previously dominated by the red alga Mazzaella laminarioides (Figure 1 a) (Jara and
Moreno, 1984). The exclusion of top predators (humans) after the creation of the Marine
Reserve in 1978, resulted in an increase in size and density of the limpet Fissurella picta
and a reduction in algal cover (Moreno et al., 1984). Algae became confined to the upper
levels of the intertidal zone where limpets do not feed (Figure 1 b) (Moreno and Jaramillo,
1983). Jara and Moreno (1984) continuously excluded F. picta from an experimental area
in the reserve with the result that the percentage cover of M. Laminarioides increased.
Thus, it would appear that the decrease in algal cover in the Reserve, after the exclusion of
human predation, was due to increased grazing by herbivores. Eight years later, by 1986,
the edible laminarian alga Durvillaea antarctica replaced the low intertidal belt of
Macrocystis pyrifera and invaded the mid intertidal of the semi-protected zones (Figure 1c),
as was described by Bustamante and Castilla (1990) in Central Chile. This change is related
to the fast growth rate of Durvillaea and its leathery consistency which reduces its
palatability to herbivores.
A similar cascade effect: humans-limpets-algae was found in the Reserve at Las
Cruces, Central Chile. After exclusion of humans, Oliva and Castilla (1986) noted a
negative relationship between abundance of the limpets F. crassa and F. limbata and algal
diversity and abundance. The abundance and diversity of macroalgae was higher outside
than inside the Reserve.

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Human exclusion has affected not only herbivores but also carnivores and their
prey. At the two Marine Reserves mentioned above, there was an increase in the biomass
of the muricid gastropod Concholepas concholepas. An increase in predation by C.
concholepas drastically reduced the density of the mussel Perumytilus purpuratus and
altered their distribution on the shore (Durán and Castilla, 1989). A reduction of mussel
abundance consequently resulted in an increase in diversity and colonization of ephemeral
algae. There are two explanations for the appearance of ephemeral algae: either predation
on mussels released space for algal colonization and/or, predation on mussels allowed
settlement of algal spores that otherwise would had been eaten by mussel filtration.
Another case has been described by Zamorano et al., (1995) in which the
opportunistic tube worm Phragmatopoma virgini recruits some years in low densities and
others in huge numbers building substantial reefs by cementing sand grains to its mucus. In
those years in which recruitment occurs at a low rate in the Marine Reserve, Concholepas
eats most of the young recruits and, in a short time most of the population disappears,
except those individuals that find refuge in crevices, whilst at the same time, in similar
areas outside the Marine Reserve sand tube reefs of Phragmatopoma form. On the other
hand, if the rate of recruitment is high, even the large predator populations inside the
Reserve, are not able to overwhelm the prey population and the sand tube reef grows
protecting the worms from further predation. In this case no differences were observed
between inside and outside the Marine Reserve (Zamorano, 1995). This case shows how
high prey recruitment may minimize the effects of predators in the organization of the
benthic assemblages. This relationship would be very difficult to interpret without knowing
the previous history of an area. As a consequence, this is not a good indicator of human
intervention.
The presence of humans alone can also cause cascade effects between trophic levels.
For example, at islands off the coasts of California (USA) and South Africa, where humans
are absent, oystercatchers maintain limpet populations at very low densities, enabling algae
to dominate. Algal beds largely are absent on the nearby mainland where the density of
oystercatchers, and hence predation pressure on limpets is much less (Frank, 1982; Hockey
and Branch, 1984). This condition would only exist where humans do not predate limpets.
Otherwise, reduction of limpets by humans would lead to a community dominated by algae.

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The processes that generate diversity in intertidal systems are generally associated
with mortality that precludes some species from becoming dominant (Paine, 1980) rather
than niche specialization. If humans are considered a disturbance agent, they cause density-
independent mortality of competing populations (Hockey and Bosman, 1986). On the other
hand, if humans are considered as part of the system, they become "keystone predators"
(Paine, 1966) causing density-dependent mortality because their effect is related to size and
abundance of their prey (Branch, 1975). Castilla (1993) used the concept of “capstone
species” for a better identification of the role of humans in the intertidal community.
Cascade effects in subtidal shores are best known for kelp communities.
Estes and Palmisano (1974) first reported that in the Aleutian Islands the sea otter Enhydra
lutris controls the abundance of the sea urchin Strongylocentrotus sp. which influences the
abundance of macroalgae. The presence or absence of sea otters determines the type of
community that will develop. The above works and Estes et al. (1982) confirmed the
paleontological evidence presented by Simenstad et al. (1978). An examination of middens
left by Aleuts indicated a negative relation between sea otters and urchins. Exploitation of
sea otters by humans caused increased herbivory leading to the destruction of kelp beds.
The re-establishment of sea otters produced a decrease in the abundance of sea urchins with
a consequent recovery of kelp beds (Duggins, 1980).

In other systems where urchins and algae are present (East Coast of Canada, West
Coast of the USA, Pacific Coast of Chile) there is no clear evidence of cascade effects and
the role of humans. Other factors such as larval recruitment, urchin behaviour, selective
predation and physical factors may produce different outcomes in the carnivore-urchin-algal
system.

Indirect effects of human predators

The preceding works present evidence of strong interactions between trophic levels.
Removal of top predators can also produce interactions within trophic levels. This indirect
effect or cross-linkage (Paine, 1980) in human-perturbed systems is only known for limpets
in Southern Chile (Godoy and Moreno, 1989). Manipulative experiments suggested that
individual growth rate and fecundity of Siphonaria lessoni are reduced in the presence of F.

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picta. High dietary overlap between these two limpets indicates that competition for food
could result if the resource is limited. Indirect effects caused by parasites, mutualistic
species pairs and weak consumer populations (i.e. Hockey, 1987; Branch and Moreno,
1994) are worth consideration for future investigations.

DISCUSSION AND PERSPECTIVES

Most of the direct and indirect effects that humans could conceivably have on
Chilean and other coastal marine ecosystems have been demonstrated. Thus, there is a need
to accept humans as part of the ecosystem, or at least to clearly recognize their influence,
when trying to establish the ecological basis for conservation.
Some scientists have taken the approach of selecting isolated, unperturbed areas to
study "natural systems". Few such areas remain in the world and they might not be
representative of the range of possible states of the various communities. Perturbed systems
are not necessarily "artificial or unnatural” and there is nothing wrong in studying them as
long as we are aware of human-induced perturbations and the research is framed in a global
context. Ignoring human perturbations in such areas might produce misleading
conclusions. For example, Santelices et al. (1981), stated that intertidal algal communities
in Chile were organized by competition, whereas Moreno and Jaramillo (1983) and Jara and
Moreno, (1984) insisted that herbivory was the organizing force. Moreno et al. (1984) and
Oliva and Castilla (1986) demonstrated that there was a high intensity of herbivore removal
by humans in Chile. On closer examination, it turned out that Santelices et al. (1981)
worked at a site where humans had removed the herbivores, whereas Jara and Moreno
worked in a marine reserve where herbivores were abundant. There was a conflict between
these studies until the above ecologists recognized that they were working with alternative
states of community dynamics resulting from different intensities of human perturbation. It
is clear now that both groups of researchers described adequately the system they were
working on. Recognizing human perturbation allowed them to accept that their results were
not contradictory but complementary. Similarly, studies of Caribbean reef communities

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previously thought as typical, were conducted on overfished areas (Hay, 1984). Thus, there
is a need in all such studies to evaluate the magnitude, location, and history of human-
induced changes in marine communities.
The increase of perturbations as a result of human utilization of marine resources for
food, ornamentation, recreational or industrial purposes, will continue to affect marine
communities. The construction of a new highway along the south part of Central Chile in
the next few years is likely to introduce many significative changes in the intertidal
communities. The study of what is happening in the intertidal communities of this
threatened zone is crucial for the future conservation and management of marine resources.
This part of the country has a longitudinal extension of 560 Km. (38°SL – 43°SL) with 408
Km. of rocky intertidal along the Eastern Pacific Ocean.
Humans are just another animal species and as such they act as selective predators
collecting or feeding on other organisms at all levels of the trophic chain. They can modify
the environment to alternative structural states. Humans can act as agents of change now,
just as they, or other factors, did in the past. Communities influenced by human intervention
are not artificial but natural. If we include humans as part of a constantly changing,
dynamic ecosystem, we can firstly learn how to interpret the processes organizing
communities among a wide range of possible states, or at least explain avoid any
discrepancies when comparing patterns of community structure, and also manage marine
resources based on sound ecological knowledge. In other words, we have nothing to lose
and much to gain. But the success of such an approach needs to start with an early
recognition of the importance of human intervention. In this context this review reveals the
following intertidal characteristics as the most clear patterns of human influence on the
rocky intertidal of Central and Southern Chile:
1. Size distributions of edible invertebrates are truncated in the larger size classes (mainly
in Fissurella spp. and Concholepas concholepas) in a range of intertidal habitats
impacted by humans (Moreno et al., 1984; Oliva and Castilla, 1986; Castilla and Durán,
1985; Moreno et al., 1986; Durán and Castilla, 1989). The exploitation of these species
drives the midlittoral community to the next pattern.
2. High cover of Mazzaella laminarioides and Ulva spp. develops in the midlittoral of
protected and semi-protected rocky shores in the absence of limpets. In transitional

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zones between sandy and rocky beaches, sand abrasion prevents the presence of limpets,
producing a similar effect as humans predators. Also, Perumytilus purpuratus has high
cover percentage and its populations form two or three layers when carnivores have
been removed by humans in rocky habitats (Moreno et al., 1984 , 1986; Durán and
Castilla, 1989). In transitional zones the sand abrasion prevents the establisment of
benthic carnivores, allowing mussel beds over isolated rocks at the border between sand
and rocky habitat (Moreno, 1995).
3. Large plants of Durvillaea antarctica are present only in the very low intertidal or
shallow subtidal rocks of exposed shores, and absent from protected and semi-protected
beaches (Castilla and Bustamante, 1989; Bustamante and Castilla, 1990).

These are the most easily perceived effects of humans on rocky intertidal communities
along central and southern Chile. The distribution of intertidal species and environmental
conditions in northern Chile and in the more southerly fjord region differ from the systems
where experimental human exclusion studies were conducted. Thus, the indicators proposed
above can only be used from Valparaíso to Chiloé. Indicators of human use for the rest of
the Chilean territory are urgently needed, especially for the northern and southernmost
zones, where exploitation of intertidal communities has become more intense and
persistent.

ACKNOWLEDGEMENTS

The author thanks W. Duarte, S. Ortega, M. Fernández, S. Petranek for reviewing early
version of the manuscript. Also I thank the help received from Dr. John M. Baxter and two
referees. This study was possible thanks to the full financial support of FONDAP
Oceanografía y Biología Marina # 3.

REFERENCES

Acuatic Conserv: Mar. Freshw.Ecosyst. 11: 19-30 (2001)

 16

Allison GW, Lubchenco J, Carr MK. 1998. Marine reserves are necessary but not sufficient
for marine conservation. Ecological applications 8(1): S79-S92.
Andrews MV, Gilberton DD, Kent M, Mellars PA. 1985. Biometric studies of
morphological variation in the intertidal gastropods Nucella lapillus (L):
Environmental and palaeoeconomic significance. Journal of Biogeography 12:
71-87.
Avery G, Siegfried WR. 1980. Food gatherers along South Africa’s seashores. Oceans, 13:
33-37.
Branch GM, Moreno CA. 1994. Intertidal and Subtidal Grazers (chapter 5) . In
W.R.Siegfried (Ed.), Rocky Shores: Exploitation in Chile and South Africa.
Ecological Studies 103. Springer-Verlag pp: 75- 100.
Branch GM. 1975. Notes on the ecology of Patella concolor and Cellana capensis, and the
effects of human consumption on the limpet population. Zoologica Africana 10:
75-85.
Brown JH, Gibson AC.. 1983. Biogeography. The C.V. Mosby Company. St Louis, MO,
USA. 643 pp.
Bustamante RH, Castilla JC. 1990. Impact of Human Exploitation on Population of the
Intertidal Southern Bull-kelp Durvillaea antarctica (Phaeophyta, Durvilleales) in
Central Chile. Biological Conservation 52: 205-220.
Castilla JC. 1993. Humans: Captone strong actors in the past and present coastal ecological
play. In McDonnell MJ, Pickett STA (Eds) Human as components of Ecosystems:
The ecology of Subtle human effects and populated areas. Springer-Verlag, New
York. pp:158-162.
Castilla JC, Durán LR. 1985. Human exclusion from the rocky intertidal zone of
central Chile: the effects on Concholepas concholepas (Gastropoda).
Oikos 45 : 391-399.
Castilla JC, Bustamante RH. 1989. Human exclusion from rocky intertidal of Las Cruces,
central Chile: effects on Durvillaea antarctica (Phaeophyta, Durvilleales). Marine
Ecology Progress Series 50: 203-214.
Castilla JC. 1999. Coastal marine communities: trends and perspectives from human-
exclusion experiments. Trends in Ecology and Evolution 14: 280-283.
Castilla JC, Fernández M. 1998. Small-scale benthic fisheries in Chile: on co-management
and sustainable use of benthic invertebrates. Ecological Applications 8(1): S124-
S132.
Connell JH. 1961. Effects of competition, predation by Thais lapillus, and other factors on
the distribution on natural populations of the barnacle Balanus balanoides.
Ecological Monographs 40: 49-78.
Connell JH. 1972. Community interactions on marine marine rocky intertidal shores.
Annual review in Ecology and Systematic 3: 169-192.
Connell JH, Sousa WP. 1983. On the evidence needed to judge ecological stability or
persistence. The American Naturalist 121-789-824.
Davis A, Moreno CA. 1995. Selection of substrata by juveniles Choromytilus chorus
(Mytilidae): are chemical cues important ?. Journal of Experimental Marine
Biology and Ecology 191: 167-180.
Dillehay TD. 1984. A late ice-age settlement in southern Chile. Scientific American 251:
100-109.

Acuatic Conserv: Mar. Freshw.Ecosyst. 11: 19-30 (2001)

 17

Duarte WE, Asencio G, Moreno CA. 1996. Long-term changes in population density of
Fissurella picta and Fissurella limbata in the Marine Reserve of Mehuin, Chile.
Revista Chilena de Historia Natural 69 (1): 45-56.
Duggins DO. 1980. Kelp beds and the sea otter: an experimental approach. Ecology 61
(3) : 447-453.
Durán LR, Castilla JC. 1989. Variation and persistence of the middle rocky intertidal
community of central Chile, with and without human harvesting. Marine Biology,
103, 555-562.
Durán LR, Castilla JC, Oliva D. 1987. Intensity of human predation on rocky shores at Las
Cruces, Central Chile. Environmental Conservation 14: 143-149.
Estes JA, Palmisano JF. 1974. Sea otters: Their role in structuring nearshore communities.
Science 185: 1058-1060.
Estes JA, Jameson RJ, Rhode EB.1982. Activity and prey selection in the sea otter:
influence of population status on community structure. The American Naturalist
120 : 242-258.
Frank PW. 1982. Effects of winter feeding on limpets by black oystercatchers,
Haematopus bachmani . Ecology 63: 1352-1362.
Godoy C, Moreno CA. 1989. Indirect effects of human exclusion from the rocky intertidal
in southern Chile: a case of cross-linkage between herbivores. Oikos 54 : 101-106.
Guénette S, Lauck,T. Clark C. 1998. Marine Reserves: from Beverton and Holt to the
present. Reviews in Fish Biology and Fisheries 8(3): 251-272.
Hay M.E. 1984. Patterns of fish and urchins grazing on caribbean coral reefs: Are previous
results typical. Ecology 65: 446-454 .
Hockey PAR, Bosman AL. 1986. Man as an intertidal predator in Transkei : disturbance,
community convergence and management of a natural food resource. Oikos 46 : 3-
14.
Hockey PAR. 1987. The influence of coastal utilization by man of the presumed extintion
of the canarian Black Oystercatcher Haematopus meadewaldoi Bannermann.
Biological Conservation 39 : 49-62.
Hockey PAR. Branch GM. 1984. Oystercatchers and limpets: impact and implications. A
preliminary assessment. Ardea 72: 199-206.
Hockey PAR. Bosman AL, Siegfried WR. 1988. Patterns and correlates of shellfish
exploitation by coastal people of Transkei: An enigma of protein production.
Journal Appl. Ecol. 25: 353-363.
Jara HF, Moreno CA. 1984. Herbivory and Structure in a midlittoral rocky community: A
case in southern Chile. Ecology 65 : 28-38.
James FC, McCulloch CE. 1990. Multivariate analysis in ecology and systematics: panacea
or Pandora’s box?. Annual Review of Ecology and Systematics 21: 129-166.
Jerardino A, Castilla JC, Ramírez JM, Hermosilla N. 1992. Early coastal subsistence
patterns in Central Chile: A systematic study of the marine-invertebrate fauna from
the site of Curaumilla-1. Latin American Antiquity 3 (1): 43-62.
Keough MJ, Quinn GP. 1991. Causality and the choice of measurements for detecting
human impacts in marine environments. Australian Journal of Marine and
Freshwater Research 42: 539-554.
Kirch PV. 1983. Man's role in modifying tropical and subtropical polynesian Ecosystems.
Archaeology in Oceania 18: 26-31.

Acuatic Conserv: Mar. Freshw.Ecosyst. 11: 19-30 (2001)

 18

Lasiak T. Dye A. 1989. The ecology of the Brown Mussel Perna perna in Transkei,
Southern Africa; Implications for the management of a traditional food resource.
Biological Conservation 47: 245-257.
Lubchenco J. 1978. Plant species diversity in a marine intertidal community, importance of
herbivore preferences and algal competitive abilities. The American Naturalist,
112: 23-39.
Menge BA, Sutherland JP. 1976. Species diversity gradients, synthesis of the roles of
predation, competition and spatial heterogeneity. The American Naturalist 110:
351-369.
Menge BA, Sutherland JP. 1987. Community regulation, variation in disturbance,
competition and predation in relation to environmental stress and recruitment. The
American Naturalist, 130: 730-757.
Montane, J .1964. Fechamiento tentativo de la ocupación humana en dos terrazas a lo largo
del litoral chileno. Arqueología de Chile Central y Areas Vecinas. En: Tercer
Congreso Internacional de Arqueología de Chile. Viña del Mar, Chile. pp: 69-107.
Moore, J.A. 1985. Science as a way of knowing: Human Ecology. American Zoologist 25 :
483-637.
Moreno CA. 1993. Efecto de la intervención humana en la mantención de la Asociación
Gymnogongrus – Choromytilus en comunidades intermareales del Sur de Chile.
Ph.D. Thesis. Pontificia Universidad Católica de Chile. Facultad de Ciencias
Biológicas. Santiago. Pp 136.
Moreno CA 1995. Benthic macroalgae as a refuge from predation for recruits of the mussel
Choromytilus chorus (Molina, 1782) in Southern Chile. Journal of Experimental
Marine Biology and Ecology 191: 181-193.
Moreno CA, Jaramillo E. 1983. The rol of grazers in the zonation of intertidal macroalgae
of the Chilean coast. Oikos 40 : 73-76.
Moreno CA, Lunecke KM, Lépez MI. 1986. The response of an intertidal Concholepas
concholepas (Gastropoda) population to protection from Man in southern Chile
and the effects on benthic sessile assemblages. Oikos 46 : 359-364.
Moreno CA, Sutherland JP, Jara HF.1984. Man as a predator in the intertidal zone of
southern Chile. Oikos 42 : 155-160.
Moreno CA, Rubilar PS.1997. Densidad de poblaciones protegidas en Reservas Marinas:
cambios en el tiempo y eventual efecto de la explotación. Estudios Oceanológicos
16: 41-50.
Newman LC, Parkes, EVH, Thompson RC. 1993. The effect of shell collecting on the
abundance of gastropds on Tanzanian shores. Biological Conservation 63: 241-
245.
Newell RC. 1979. Biology of intertidal animals. Marine Ecological Survey Ltd. Faverham,
Kent. UK. 757 pp.
Oliva D, Castilla JC. 1986. The effect of human exclusion on the population structure of
key-hole limpets Fissurella crassa and F.limbata on the coast of central
Chile. P.S.Z.N.I: Marine Ecology 7 : 201-217.
Ortega S. 1987. The effect of human predation on the size distribution of Siphonaria
gigas (Mollusca : Pulmonata) on the Pacific Coast of Costa Rica. The
Veliger 29 : 251-255.
Paine RT. 1966. Food web complexity and species diversity. American Naturalist 100 :
65-75.

Acuatic Conserv: Mar. Freshw.Ecosyst. 11: 19-30 (2001)

 19

Paine RT. 1976. Size-limited predation:an observation and experimental approach with the
Mytilus-Pisaster interaction. Ecology 57 : 858-873.
Paine RT. 1980. Food webs: Linkage, interaction strengh and community infraestructure.
Journal of Animal Ecology 49 : 667-685.
Parkington J. 1977. Coastal settlement between the mouths of the Berg and Olifant rivers,
Cape Province. S. Afr. Archaeol. Bull. 31 : 127-140.
Parra B. Moreno CA, Westermeier R. 1992. Anthropogenic effects on the community
structure of intertidal algae of the Valdivian coast. In Ulrich Seeliger (Ed) Costal
Plant Communities of Latin America , Academic Press Inc. USA. pp 65-76
Rafaelli D, Hawkins S. 1996. Intertidal Ecology. Chapman & Hall, London. pp 355.
Rowley RJ, 1994. Marine Reserves in fishery management. Aquatic Conservation: Marine
and Freshwater Ecosystems, 4 : 233-254.
Salm R, Price A. 1995. Selection of Marine Protected areas. In S. Gubbay (Ed) Marine
protected Areas. Chapman and Hall (London). pp:232.
Santelices B, Montalva S, Oliger P. 1981. Competitive algal community organization in
exposed intertidal habitat from Central Chile. Marine Ecology Progress Series
6 : 267-276.
Schippacasse V, Niemeyer H. 1964. Excavaciones de un conchal en el pueblo de
Guanaqueros (Prov. de Coquimbo). En: Tercer Congreso Internacional de
Arqueología de Chile, Viña del Mar, Chile. pp: 235-262.
Seed R. 1976. Ecology. In: BL Bayne (ed) Marine mussels: their ecology and physiology.
Cambridge University Press, Cambridge UK, pp: 13-66.
Seed R, Suchaneck TH. 1992. Population and community ecology of Mytilus. Chapter 4 In
E. Gosling (Ed.) The mussel Mytilus: Ecology, Physiology, Genetics and Culture.
Elsevier, Amsterdam. Pp 87-169.
Siegfried WR, Hockey PAR, Crowe AA. 1985. Exploitation and Conservation of Brown
Mussels stocks by Coastal People of Transkei. Environmental Conservation 12 :
303-307.
Sih AP, Crowley M, McPeek J, Petranka J, Strohmeier K. 1985. Predation, competition
and prey communities: A review of field experiments. Annual Review of
Ecology and Systematics 16 : 269-311.
Simenstad CA, Estes JA, Kenyen KL. 1978. Aleuts, Sea Otters, and Alternate Stable-State
Communities. Science 200 : 403-411.
Sousa WP 1979. Disturbance in marine intertidal boulder fields: the non-equilibrium
maintenance of species diversity. Ecology, 60, 1225-1239.
Speed E. 1969. Prehistoric shell collectors. Soth African Archaeological Bulletin 24: 193-
196.
Underwood AJ, Denley EJ. 1984. Paradigms, explanations and generalization in models for
the structure of intertidal communities on rocky shores, In Ecological Communities,
Conceptual Issues and the Evidence. Eds Strong DR, Simberlof D, Abele LG,
Thistle AB. Princeton University Press, Princeton, NH, pp 151-180.
Zamorano J. 1995. Efecto de la depredación sobre la distribución y abundancia de
Phragmatopoma virgini Kinberg 1867 (Polychaeta; Sabellaridae), en el intermareal
rocoso de Mehuín, Sur de Chile. Master Science Thesis, Ecology. Universidad
Austral de Chile. Pp: 125.

Acuatic Conserv: Mar. Freshw.Ecosyst. 11: 19-30 (2001)

 20

Zamorano J, Moreno CA, Duarte WE. 1995. Post-settlement mortality in Phragmatopoma

virgini Kinberg, 1867 (Polychaeta: Sabellaridae) at the Mehuin Marine Reserve.
Marine Ecology Progress Series 127 : 149-155.
Zedler JB.1978. Public use effects in the Cabrillo National Monument intertidal zone.
Project Report. U.S.Department of Interior National Park Service. pp: 27.

Figure Caption

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Figure 1. Three states of the benthic assemblage in the semi-exposed intertidal in southern
Chile. A). High algae abundance in the mid intertidal when humans remove
herbivores. B). Short term ecological answer to human exclution, when key-hole
limpets increase their abundance and over-exploit all palatable algae and, C) After
eight years of human exclusion, Durvillaea antarctica outcompetes Macrocystis
and invades the mid-intertidal in wave semi-exposed and exposed fronts.

Acuatic Conserv: Mar. Freshw.Ecosyst. 11: 19-30 (2001)