Realistic losses of rare species disproportionately impact higher trophic levels

L E T T E RRealistic losses of rare species disproportionately impact higher

trophic levels

Matthew E. S. Bracken1* and

Natalie H. N. Low2

1Marine Science Center,

Northeastern University, 430 Nahant

Road, Nahant, MA 01908, USA2Department of Ecology and

Evolutionary Biology, Brown

University, 80 Waterman Street,

Providence, RI 02912, USA

*Correspondence: E-mail:

[email protected]

AbstractPredicting the consequences of changes in biodiversity requires understanding both species� susceptibility to

extirpation and their functional roles in ecosystems. However, few studies have evaluated the effects of realistic,

non-random biodiversity losses, severely limiting the applicability of biodiversity research to conservation.

Here, we removed sessile species from a rocky shore community in a way that deliberately mimicked natural

patterns of species loss. We found that the rarest species in the system act from the bottom up to

disproportionately impact the diversity and abundance of consumers. Realistic losses of rare species in a diverse

assemblage of seaweeds and sessile invertebrates, collectively comprising <10% of sessile biomass, resulted in a

42–47% decline in consumer biomass. In contrast, removal of an equivalent biomass of dominant sessile

species had no effect on consumers. Our results highlight the �cornerstone� role that rare species can play in

shaping the structure of the community they support.

KeywordsBiodiversity, consumer, cornerstone species, herbivory, rare species, rocky intertidal, seaweed.

Ecology Letters (2012) 15: 461–467

INTRODUCTION

Given global threats to biodiversity (Butchart et al. 2010; Barnosky

et al. 2011), understanding the consequences of biodiversity loss is of

utmost importance. However, the majority of research into the

functional consequences of diversity change is based on biodiversity

gradients constructed of randomly assembled communities of

organisms. Whereas this approach has contributed a great deal to

our understanding of the mechanisms linking biodiversity to

community and ecosystem properties (Hooper et al. 2005; Cardinale

et al. 2006), it is limited in its applicability to natural systems, where

changes in the number and relative abundance of species are not

random (Hutchinson 1959; Menge & Sutherland 1987). Increasing

attention is being paid to realistic species-loss scenarios (e.g. Smith &

Knapp 2003; Solan et al. 2004; Zavaleta & Hulvey 2004), and recent

work has highlighted striking differences in the effects of random vs.

realistic species losses (Bracken et al. 2008).

Progress in understanding how a species� susceptibility to loss is

related to its functional role in a community or ecosystem is essential if

we are to make biodiversity research relevant to conservation (Schwartz

et al. 2000; Srivastava & Vellend 2005). Accomplishing this will require

focusing simultaneously on both the causes and the consequences of

biodiversity change. Here, we link realistic changes in biodiversity to

community structure and species interactions by using natural variation

in diversity at the base of a marine food web to evaluate (1) the

relationships between sessile diversity and consumer diversity and

abundance and (2) the effects of realistic declines in sessile diversity on

higher trophic levels. In our initial surveys of a coastal rocky shore

community, we found that patterns of sessile richness occurred in a

nested order: a few common dominant species were present in all

surveyed plots, whereas several rare species – up to eight additional

species in the most diverse plots, collectively comprising <10% of

sessile biomass – were present only in high-diversity plots.

Both the abundance and diversity of consumers were higher in plots

containing more sessile species (see Results), and we hypothesised that

the rare seaweeds and sessile invertebrates that were uniquely present

in more diverse plots were facilitating those consumers. Species at the

base of a food web often provide both food and habitat for organisms

at higher trophic levels (Pimm 1980; Hunter & Price 1992; Knops

et al. 1999). However, previous work has largely focused on how

sessile species� roles are associated with their abundance (Lindeman

1942; Hutchinson 1959; Oksanen et al. 1981; Hairston & Hairston

1993). For example, dominant, foundation species (sensu Dayton

1972) enhance the diversity and abundance of organisms by providing

physical structure (Ellison et al. 2005; Bracken et al. 2007), and high

biomass of organisms at the base of a food web is typically required to

ensure sufficient energy flow to consumers (Elton 1927; Lindeman

1942; Paine 1980). However, few studies have empirically assessed the

effects of the loss of rare species from the base of food webs (but see

Marsh et al. 2000; Lyons & Schwartz 2001; Zavaleta & Hulvey 2004),

although these rare species often constitute the majority of species

richness in communities (Gotelli & Graves 1996; Novotny & Basset

2000).

We tested our hypothesis that realistic declines in rare species can

impact higher trophic levels by experimentally reducing the number of

rare seaweed and sessile invertebrate species on rocky intertidal reefs

so that richness and composition of experimental removal plots

mimicked values found in naturally occurring low-richness control

plots. We also conducted laboratory mesocosm experiments to

evaluate the preferences of the most common consumer at our study

location for rare vs. abundant seaweed species in our field plots. By

combining field observations and experiments with studies of

herbivore preferences, we document the importance of rare species

in shaping community structure from the bottom-up, mediating the

diversity, and especially the abundance, of organisms at higher trophic

levels.

Ecology Letters, (2012) 15: 461–467 doi: 10.1111/j.1461-0248.2012.01758.x

� 2012 Blackwell Publishing Ltd/CNRS

MATERIALS AND METHODS

Initial surveys

In early July of 2010, we marked 30 permanent square plots

(25 · 25 cm) in the mid-intertidal zone of a moderately wave-exposed

rocky reef at East Point, Nahant, Massachusetts, USA

(42º25¢00.71¢ N, 70º54¢19.23 W). Plots spanned approximately

100 m of shoreline, and community structure did not differ with

distance along the shore, suggesting that no underlying gradients (e.g.

wave energy) were responsible for variation in diversity in our plots.

We initially surveyed plots on 4 July 2010 to estimate per cent cover

of macroalgae and sessile invertebrates and count mobile inverte-

brates. Sessile invertebrates included the barnacle Semibalanus balanoides

L., the mussel Mytilus edulis L., the sea anemone Haliplanella lineata

Verrill, and the hydroid Dynamena pumila L., Macroalgae included the

Heterokontophytes Fucus vesiculosus L. and Ascophyllum nodosum (L.)

Le Jolis; the Rhodophytes Hildenbrandia rubra (Sommerfelt) Meneghini,

Mastocarpus stellatus (Stackhouse) Guiry, Chondrus crispus Stackhouse,

Vertebrata lanosa (L.) T. A. Christensen, Dumontia contorta (S. G. Gmelin)

Ruprecht, Porphyra umbilicalis Kutzing, and coralline crusts

[e.g. Clathromorphum circumscriptum (Stromfelt) Foslie]; and the Chloro-

phytes Ulva lactuca L. and Cladophora rupestris (L.) Kutzing (Fig. 1a).

Mobile invertebrates included the herbivorous littorine snails Littorina

littorea L., Littorina obtusata L., Littorina saxatilis Olivi, and Lacuna vincta

Montagu; the herbivorous limpet Testudinalia testudinalis O. F. Muller;

the amphipod Gammarellus angulosus Rathke; the predatory dogwhelk

Nucella lapillus L.; the omnivorous shore crab Hemigrapsus sanguineus

De Haan; and juveniles of the predatory crab Carcinus maenas L.

Diversity loss experiments

Plots were surveyed a second time, on 6 July 2010, to count mobile

invertebrates prior to initiation of experimental species removals on 8

July 2010. On the basis of our initial surveys, we ranked 30

experimental plots according to sessile richness (Fig. 1a). We

designated the n = 10 lowest-richness plots as un-manipulated, �Low

Richness Controls�. We randomly assigned each of the 20 high-

richness plots to one of two treatments: un-manipulated �High

Richness Control� plots (n = 10) or �Experimental Diversity Loss�plots (n = 10). We removed species from Diversity Loss plots so that

the richness and composition of those plots mimicked Low Richness

Controls (see Fig. S1 in Supporting Information). The distribution of

plot treatments along the shore was indistinguishable from a random

assignment of treatments (P = 0.620).

We experimentally reduced sessile species richness in Diversity Loss

plots by selectively removing species that were uniquely present in

plots containing ‡5 species, with the exception of coralline crusts,

which were impractical to remove. By restricting our manipulations to

those species that were absent in nearby low-diversity plots, our

experiment imposed a realistic pattern of species loss on the

ecosystem. Species removed included the hydroid Dynamena and the

macroalgae Ascophyllum, Mastocarpus, Chondrus, Dumontia, Ulva and

Cladophora. Note that despite being present in one high-richness plot,

Porphyra was not removed because that plot was assigned to a High

Richness Control treatment. And one Experimental Diversity Loss

plot – the least diverse of the 20 high-richness plots – contained no

removable species that were uniquely present in high-richness plots.

Sessile species richness and composition in Diversity Loss plots

therefore became deliberately similar to levels in the Low Richness

Control plots, simulating a realistic loss of sessile species from the

local community. Organisms removed from plots were separated,

dried (60 �C to constant mass) and weighed. On the basis of

regressions between cover and sessile biomass at the end of the

experiment (see below), we back-calculated the total sessile biomass

prior to removals. The biomass removed from the plots averaged

9.9 ± 3.7 (mean ± SE) per cent of total sessile biomass. To maintain

treatments, Diversity Loss plots were weeded once a week, as

necessary, which consisted mostly of removing small amounts of fast-

growing ephemeral seaweed species, with minimal disturbance to

plots. During the removal experiment, we surveyed macroalgae and

sessile invertebrates (% cover; note that because of layering of canopy

and understory species, cover often exceeded 100%) and mobile

consumers (count) in the plots from 11 July to 12 August 2010.

At the conclusion of the experiment, we removed all mobile

invertebrates, sessile invertebrates and macroalgae from plots, sorted

them in the lab, and determined their dry mass (60 �C to constant

mass) and ash-free dry mass (500 �C for 24 h, subtracted from dry

mass). We used the biomass of sessile invertebrates and macroalgae

from each plot to verify that cover was a good surrogate for biomass

(R2 = 0.77, P < 0.001). Mobile invertebrates were separated to

species, and we used the average ash-free dry biomass of each species

in each plot to convert the counts from our surveys to biomass values.

(a)

(b)

(c)

Figure 1 Changes in sessile species composition and consumer biomass with

increasing sessile species richness. (a) As sessile species richness increased, common

dominant macroalgae (M) and sessile invertebrates (I) were supplemented by a

diverse assemblage of rare sessile species, which collectively comprised <10% of

sessile biomass. Plots containing more sessile species were characterised by greater

consumer (b) richness (P = 0.002, R2 = 0.28) and (c) biomass (P < 0.001,

R2 = 0.44).

462 M. E. S. Bracken and N. H. N. Low Letter


Although very little biomass was removed from Diversity Loss

plots, we evaluated the potential effects of biomass removal in two

ways. First, we evaluated relationships between the change in

consumer biomass in removal plots during the summer of 2010

[(final survey on 12 August 2010)–(initial survey on 4 July 2010)] and

both the amount of sessile biomass removed and the number of

sessile species removed.

We also conducted a follow-up experiment to assess whether the

minimal disturbance associated with removals could have affected

consumers. During the summer of 2011, we repeated our field

experiment with an additional treatment, the removal of biomass of

the abundant species present in all plots (i.e. regardless of sessile

richness) without actually reducing sessile richness. The biomass

removed from these Disturbance Controls was equivalent to the

biomass of the less abundant species that was removed in Experi-

mental Diversity Loss treatments. This experiment included 36 plots:

High Richness Controls (n = 9), Disturbance Controls (n = 9),

Experimental Diversity Loss plots (n = 9) and Low Richness Controls

(n = 9). Plots were initially surveyed on 30 July 2011, and removals

were conducted on 2 August 2011. An average of 6.2 ± 2.3

(mean ± SE) g dry biomass was removed from Diversity Loss plots,

and 6.5 ± 0.7 g was removed from Disturbance Control plots; the

amounts removed did not differ between treatments (t-test: P = 0.902)

and represented approximately 6% of total sessile biomass in each

removal plot. Biomass removals for common species involved

thinning the dominant macroalga Fucus and sessile invertebrates

Mytilus and Semibalanus. The experiment was maintained, and plots were

surveyed weekly, until 9 September 2011. Note that the experiment

was preceded by a series of heat waves (e.g. National Climatic Data

Center 2011) that coincided with daytime low tides, which caused

many mobile consumers to seek refuge lower on the shore and led to

low overall consumer richness and abundance in our early surveys.

Consumer preference experiment

We evaluated herbivore growth rates and preferences for abundant vs.

rare seaweeds by measuring consumption and growth rates of the

most common herbivore in our experimental plots, the snail

L. obtusata, using no-choice and multiple-choice grazing experiments.

The experiment was conducted in 0.7-L perforated transparent plastic

mesocosms placed in outdoor tanks plumbed with unfiltered running

seawater. Each mesocosm was divided into two halves by a plastic

mesh screen that separated the experimental snail-addition side from

the no-snail control side. We placed 6 g of seaweed in both sides of

every mesocosm and added 5 g (wet mass, equivalent to approx-

imately 7 individuals) of snails to one, randomly selected side of each

mesocosm. We measured grazing rates in n = 10 replicates each of

seven different treatments: each seaweed species by itself and all six

species (Fucus, Ascophyllum, Cladophora, Mastocarpus, Ulva and Chondrus)

together. Grazing was assessed by comparing, for each species, the

change in algal biomasses on each side of each mesocosm. Values are

reported as the difference in % biomass lost over 4 days in treatments

with and without snails.

Statistical analyses

We analysed our data using general linear models, generalised linear

models (i.e. logistic regression to evaluate whether Cladophora, a

preferred seaweed species, occurred more often in more diverse plots)

and t-tests after verifying that the data met assumptions of normality

and homogeneity of variances. In the multiple-choice grazing

experiment, algal species in each chamber were not independent of

one another, so comparisons between species were made using paired

t-tests. We assessed changes in sessile and mobile consumer

community composition along the shore by conducting non-metric

multidimensional scaling (MDS) analyses based on square-root

transformed data with the Bray-Curtis measure of similarity. Analyses

were conducted using SAS version 9.2 (SAS Institute 2008) and

PRIMER version 6 (Clarke & Gorley 2006).

RESULTS

Initial surveys

We verified that underlying gradients along the shore were not

responsible for variation in diversity in our experimental plots by

evaluating relationships between distance and sessile species cover

(F1,28 = 2.9, P = 0.100), sessile species richness (F1,28 = 0.0,

P = 0.996), sessile species evenness (F1,28 = 2.4, P = 0.125), con-

sumer biomass (F1,28 = 0.0, P = 0.851), consumer richness

(F1,28 = 3.4, P = 0.078) and consumer evenness (F1,28 = 3.4,

P = 0.072). Neither sessile (stress = 0.12, F1,28 = 1.4, P = 0.241)

nor mobile consumer (stress = 0.01, F1,28 = 2.9, P = 0.101) com-

munity composition (i.e. MDS axis 1) changed with distance along the

shore.

In our surveys of 30 plots, we found that as the number of sessile

species increased, the few abundant species found in all plots (e.g. the

rockweed Fucus, the barnacle Semibalanus, and the mussel Mytilus) were

supplemented by a number of rare sessile species (up to eight

additional species in the most diverse plots; Fig. 1a). These rare

species collectively represented an average of <10% of biomass in

plots where they occurred. Increases in sessile species richness were

associated with increases in both the richness (F1,28 = 10.94,

P = 0.002, R2 = 0.28; Fig. 1b) and especially the biomass

(F1,28 = 22.1, P < 0.001, R2 = 0.44; Fig. 1c) of mobile consumer

species, suggesting that rare sessile species could facilitate mobile taxa

from the bottom up.

Diversity loss experiment

Prior to the start of our experiment, Experimental Diversity Loss

plots contained the same number of sessile species as High Richness

Control plots (t = 0.7, d.f. = 18, P = 0.518) and more species than

the Low Richness Control plots (t = 4.9, d.f. = 18, P < 0.001;

Fig. 2a). Removals caused an immediate decline in sessile richness

so that by the next survey date, sessile richness in Diversity Loss plots

matched that in Low Richness Controls (t = 0.37, d.f. = 18,

P = 0.718), but was lower than that of the un-manipulated High

Richness Controls (t = 6.95, d.f. = 18, P < 0.001). This pattern

continued for the duration of our experiment. At the same time,

sessile cover, a good surrogate for biomass in this system, never

differed among the three treatments (P > 0.05; Fig. 2b). Thus, we

experimentally achieved a 40% reduction in sessile species richness,

but the species removed were extremely rare, so removals had no

effect on the total abundance of sessile species.

After experimental removals, the richness of mobile species in

Experimental Diversity Loss plots declined rapidly relative to High

Richness Controls (Fig. 2c). At the end of the experiment, Diversity

Letter Loss of rare �cornerstone� species 463


Loss plots contained an average of 1.3 (±0.4 SE) fewer species than

High Richness Controls (t = 3.2, d.f. = 18, P = 0.003). The two

consumer species that were present in some of the Diversity Loss

plots at the beginning of the experiment but absent at the end were

Testudinalia and Nucella.

Mobile species biomass responded similarly to experimental

removals of sessile species (Fig. 2d). Prior to removals, the consumer

biomass in Diversity Loss plots was the same as biomass in High

Richness Controls (t = 0.5, d.f. = 18, P = 0.657) and higher than the

biomass in Low Richness Controls (t = 2.5, d.f. = 18, P = 0.020).

After 3 weeks, biomass of mobile species in Diversity Loss plots had

declined relative to High Richness Controls (t = 2.1, d.f. = 18,

P = 0.047) to match that in Low Richness Controls (t = 0.8,

d.f. = 18, P = 0.416). This pattern continued for the remainder of

the experiment. After 5 weeks, removal of rare species led to a 42%

reduction in mobile biomass in Diversity Loss plots relative to High

Richness Controls. Removal plots ultimately contained an average of

0.60 (±0.28 SE) g less consumer ash-free dry biomass than High

Richness Controls, which is equivalent to 25 L. obtusata (approxi-

mately 0.02 g each), 44 Testudinalia (approximately 0.01 g each), four

Nucella (approximately 0.14 g each), or nine juvenile Carcinus

(approximately 0.06 g each). Several mobile invertebrate species

independently exhibited the same pattern of changes in abundance as

the entire assemblage. These included the snail L. obtusata (the most

abundant mobile invertebrate in the plots), the limpet Testudinalia, the

dogwhelk Nucella, and juvenile green crabs (Carcinus; adult crabs were

uncommon at this wave exposure and tidal elevation) (Fig. S2).

The effect on consumer biomass was not due to the minimal

disturbance associated with Experimental Diversity Loss treatments.

The realistic loss of rare species in Diversity Loss treatments, but not

the removal of an equivalent biomass in Disturbance Controls,

disproportionately reduced consumer abundances (Fig. 3). Sessile

richness was lower in Diversity Loss plots; at the end of the

experiment, values were lower than those in High Richness Control

plots (t = 6.1, d.f. = 16, P < 0.001) and equivalent to those in Low

Richness Controls (t = 1.9, d.f. = 16 P = 0.070; Fig. 3a). Disturbance

to plots without loss of species did not affect sessile species richness,

as richness values in Disturbance Controls never differed from those

in High Richness Controls (P > 0.086). Removals never affected

sessile cover (Fig. 3b); after 5 weeks, cover in all treatments was

indistinguishable (F3,32 = 0.6, P = 0.634).

In the summer of 2011, consumer richness levels in our

experimental plots were half as high as levels observed in our 2010

experiment (High Richness Controls: t = 4.0, d.f. = 17, P < 0.001;

Low Richness Controls: t = 2.8, d.f. = 17, P = 0.013; Figs 2c and 3c),

and richness did not respond as strongly to species removals in

Experimental Diversity Loss treatments (Fig. 3c). This probably

occurred because of the severe heat wave at the end of July 2011; our

nearby intertidal temperature dataloggers, which are shaded to

eliminate effects of direct solar radiation, recorded a maximum low-

tide air temperature of 43.5 �C on 22 July 2011. Mobile richness in

Disturbance Controls was never different from richness in High

Richness Controls (P > 0.512). However, Diversity Loss plots also

never differed from High Richness Controls (P > 0.129). Whereas

mobile richness in Diversity Loss plots was initially indistinguishable

from that in Low Richness Controls (t = 1.6, d.f. = 16, P = 0.137),

richness shortly following the initiation of experimental removals was

higher in Diversity Loss plots than in Low Richness Controls

(6 August: t = 3.6, d.f. = 16, P = 0.002; 13 August: t = 3.4, d.f. = 17,

P = 0.004). Richness in Diversity Loss plots then declined relative to

High Richness Control plots to become indistinguishable from Low

Richness Controls by the end of the experiment (t = 1.4, d.f. = 16,

P = 0.185; Fig. 3c).

Biomass (g ash-free dry mass per plot) of consumers in Disturbance

Control plots was never different from that in High Richness Controls

(P > 0.192). In contrast, Experimental Diversity Loss plots initially

had higher consumer biomass than Low Richness Controls (t = 2.7,

d.f. = 16, P = 0.017) and were not different from High Richness

Controls (t = 0.3, d.f. = 16, P = 0.743). By the end of the exper-

iment, the average consumer biomass in Diversity Loss treatments

was indistinguishable from that in Low Richness Controls (t = 1.1,

d.f. = 16, P = 0.287) and 47% lower than in High Richness Controls

(t = 2.1, d.f. = 16, P = 0.049; Fig. 3d).

(a)

(b)

(c)

(d)

Figure 2 Changes in sessile richness, sessile cover, mobile richness and mobile

biomass in response to realistic removals of rare sessile species in 2010. (a) Sessile

richness in Experimental Diversity Loss plots was initially equivalent to High

Richness Controls, but declined so that it matched Low Richness Controls

following removals. (b) Diversity Loss did not affect sessile cover. (c) Mobile

richness in Diversity Loss plots was initially similar to that in High Richness

Control plots, but became indistinguishable from Low Richness Controls after

removals. (d) Consumer biomass in Diversity Loss plots was initially indistinguish-

able from High Richness Controls, but biomass became indistinguishable from Low

Richness Controls after removals. Values are means ± SE.



Additionally, we found that the amount of sessile biomass removed

from Experimental Diversity Loss plots did not affect the change in

consumer biomass (F1,8 = 0.2, P = 0.639, R2 = 0.03; Fig. 4a). Rather,

the reduction in consumer biomass associated with removals was

more pronounced in plots from which more sessile species were

removed (F1,8 = 5.5, P = 0.048, R2 = 0.41; Fig. 4b).

Grazer preference experiment

Despite consuming similar amounts of all 6 seaweed species in no-

choice trials (F5,52 = 0.7, P = 0.591), snails grew different amounts

when fed different seaweeds (F5,52 = 2.8, P = 0.025). The snail

L. obtusata only grew when fed a diet of the rare seaweed Cladophora

(one-sample t = 4.1, d.f. = 9, P = 0.003; Fig. 5a), and conversion

efficiencies (grams of snail biomass added per gram of seaweed

consumed) of snails fed Cladophora were 11.5 times higher than for

snails fed the dominant Fucus. When given a choice among all six

seaweeds, snails preferred Cladophora to the dominant Fucus (paired

t = 2.5, d.f. = 9, P = 0.036); consumption of other seaweeds did not

differ from Fucus (P > 0.12; Fig. 5b). When other seaweed species

were also present, Fucus grew better in the presence of grazers than it

did in their absence (t = 2.4, d.f. = 9, P = 0.039), leading to an

observed negative consumption rate. We used our initial surveys to

assess whether Cladophora occurred more often in plots containing

more sessile species and found that Cladophora was more likely to

occur in more diverse plots (logistic regression: v2 = 6.0, P = 0.015).

Based on biomass removed, Cladophora was approximately twice as

abundant in plots that also contained Ascophyllum (t = 2.3, d.f. = 8,

P = 0.049), which was another rare species on this moderately

exposed shoreline.

DISCUSSION

By removing rare sessile species from experimental plots in a way that

mimicked observed species losses in the system, we have shown that

realistic patterns of rare species loss can have disproportionate effects

on higher trophic levels. Specifically, removal of a diverse assemblage

of species, collectively comprising <10% of sessile biomass, resulted

in a 40–50% decline in the biomass of consumers (Figs 2d and 3d).

Thus, the rare seaweeds and sessile invertebrates present in more

diverse plots were facilitating consumers, leading to greater consumer

richness and biomass in plots containing more sessile species. Several

mobile consumers in our plots, including the herbivores L. obtusata

and Testudinalia and the carnivores Nucella and Carcinus, declined in

response to removals (Fig. S2), highlighting the community-wide

bottom-up influence of rare sessile species. Furthermore, because

both Nucella and Carcinus consume L. obtusata (Hughes & Dunkin

(a)

(b)

(c)

(d)

Figure 3 Realistic removals of rare species, but not the disturbance associated with

the loss of an equivalent biomass of common species, reduced consumer

abundances in 2011. (a) Experimental Diversity Losses, but not biomass losses in

Disturbance Controls, reduced sessile richness. (b) Neither Disturbance nor

Diversity Loss affected sessile cover. (c) Neither Disturbance nor Diversity Loss

affected mobile richness relative to High Richness Controls. (d) Consumer biomass

in Disturbance Controls was never different from High Richness Controls.

However, consumer biomass in Diversity Loss plots was initially indistinguishable

from High Richness Controls and higher than Low Richness Controls. After

removals, consumer biomass was 47% lower than High Richness Controls and

indistinguishable from Low Richness Controls. Values are means ± SE.

(a)

(b)

Figure 4 Effects of the amount of sessile biomass and the number of sessile

species removed on the change in consumer biomass in removal plots. (a) The

amount of sessile biomass removed had no effect on the change in consumer

biomass observed in removal plots (P = 0.639, R2 = 0.03). (b) Where more sessile

species were removed, there was a greater effect on consumer biomass (P = 0.048,

R2 = 0.41).



1984; Rangeley & Thomas 1987), and Carcinus consumes Nucella

(Rangeley & Thomas 1987), the effects of rare species removals

probably propagate up the food web.

The rare species removed from our plots play essential roles in

providing food (Lubchenco & Menge 1978; Long & Trussell 2007)

and ⁄ or habitat (Lubchenco 1978; Bertness et al. 1999) for these

consumers, and the fact that the effect of removals on consumer

biomass increased with the number of sessile species removed

(Fig. 4b) suggests that sessile species may act together to influence

mobile consumers. For example, the canopy of the seaweed

Ascophyllum, one of the rare species removed from our plots, reduces

temperature and desiccation stress, facilitating a variety of taxa

(Bertness et al. 1999), including another rare seaweed, Cladophora

(Ingolfsson & Hawkins 2008). Cladophora biomass was twice as high in

our removal plots that also contained Ascophyllum. Our grazer

preference experiment highlights the importance of Cladophora to

consumers; snails only grew when fed Cladophora, and they consumed

it more readily than the dominant Fucus (Fig. 5). Cladophora was more

likely to occur in plots containing more sessile species, and it was

present in most (7 ⁄ 10) of the removal plots in our 2010 experiment.

In fact, when alternative, more palatable seaweeds (e.g. Cladophora)

were available, Fucus actually grew more when grazers were present

than when absent (Fig. 5b), highlighting a potential role of herbivores

in enhancing the dominant seaweed species in a diverse assemblage.

The rapid response of consumers to removals of rare sessile species

was particularly striking. In contrast to removals of rocky intertidal

consumers, where effects on the diversity and biomass of sessile

species can take months to become apparent (Paine 1974; Castilla &

Duran 1985), we observed negative effects of the removal of sessile

species on consumer biomass and diversity within 3 weeks. Effects of

consumer removals are mediated by recruitment of sessile species

(Paine 1974; Castilla & Duran 1985; Menge et al. 1994), whereas

mobile consumers can rapidly emigrate in search of higher quality

food (Root 1973; Levinton & Kelaher 2004). Especially at small spatial

scales such as the plot sizes in our experiment, the movement of

mobile organisms away from suboptimal habitats, demonstrated both

here and in prior work (Parker & Stuart 1976; Levinton & Kelaher

2004), adds an under-appreciated behavioural dimension to our

understanding of the bottom-up consequences of species loss. At

larger spatial scales, rarity of palatable food sources is probably

mediated, at least in part, by consumers.

The rare species we removed had large and disproportionate effects

on higher trophic levels, and therefore acted similarly to keystone

species in their effect on community structure (Power et al. 1996).

There is no theoretical reason why keystone species cannot operate

from anywhere in a food web (Pimm 1982). However, the term, as

originally defined by Paine (1969), generally refers to predators. We

therefore call rare species that have large and disproportionate

bottom-up effects on consumers �cornerstone species� to differentiate

them from both keystone predators (Paine 1969, 1974) and

foundation species (Dayton 1972; Ellison et al. 2005). Architecturally,

a keystone represents a relatively small portion of an arch, but

determines its stability and function from the top-down, and a

foundation supports a structure from the bottom-up, but by virtue of

its mass. A cornerstone represents a relatively small portion of a

foundation, but defines the shape of the structure above it.

We removed species in a way that mimicked realistic species losses in

the system – our removal treatments were specifically designed to match

naturally occurring low-richness plots – demonstrating the importance

of rare species as mediators of community structure and dynamics. We

show that large and disproportionate effects of rare species can act not

only from the top-down, as several previous studies have demonstrated

(Power et al. 1996), but also from the bottom-up, influencing the

richness and especially the abundance of other organisms in a

community (see also Nason et al. 1998). With respect to conservation

priorities in an era of global biodiversity change (Butchart et al. 2010),

understanding the factors that influence biodiversity is critical. Here,

a suite of inconspicuous species maintains rocky intertidal community

structure, and this effect increases with their diversity. It is not just

common, dominant species that mediate abundance and diversity at

higher trophic levels (e.g. Ellison et al. 2005; Gaston & Fuller 2008). Rare

species act as the cornerstones of this community, comprising relatively

little biomass, but dictating the shape of the community they support.

ACKNOWLEDGEMENTS

We thank C. Bracken-Sorte, A. Drouin, V. Perini, S. Trieweiler, and

students in the Three Seas Program for assistance in setting up and

maintaining experiments. B. Menge, E. Sanford, C. Sorte, J.

Stachowicz, G. Trussell, T. Wootton and anonymous referees

provided helpful comments on the manuscript. This work was

funded by the National Science Foundation (OCE-0961364 to M. E.

S. B. and G. Trussell). This is contribution number 280 of the

Northeastern University Marine Science Center.

AUTHOR CONTRIBUTION

MESB and NHNL designed and performed the research; MESB

analysed the data and wrote the paper; and both MESB and NHNL

contributed substantially to revisions.

(a)

(b)

Figure 5 Grazing and growth rates of snails feeding on different seaweeds. (a) When

snails were offered each seaweed by itself, they consumed an equivalent amount of

the tissue of each species (ANOVA: P = 0.591). However, their growth depended on

the species provided (ANOVA: P = 0.025). Specifically, snail growth only occurred

when snails were fed Cladophora. (b) Snails that were given all six seaweed species at

the same time consumed more Cladophora than they did Fucus. Asterisks (*) indicate

rare species (a) on which snails grew or (b) which were consumed at higher rates than

the dominant Fucus (P < 0.05). Values are means ± SE.



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Realistic losses of rare species disproportionately impact higher trophic levels