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Habitat Loss, Trophic Collapse, and the Decline of Ecosystem Services Author(s): Andrew Dobson, David Lodge, Jackie Alder, Graeme S. Cumming, Juan Keymer, Jacquie McGlade, Hal Mooney, James A. Rusak, Osvaldo Sala, Volkmar Wolters, Diana Wall, Rachel Winfree, Marguerite A. Xenopoulos Source: Ecology, Vol. 87, No. 8 (Aug., 2006), pp. 1915-1924 Published by: Ecological Society of America Stable URL: http://www.jstor.org/stable/20069174 Accessed: 13/03/2009 15:28 Your use of the JSTOR archive indicates your acceptance of JSTOR's Terms and Conditions of Use, available at http://www.jstor.org/page/info/about/policies/terms.jsp. JSTOR's Terms and Conditions of Use provides, in part, that unless you have obtained prior permission, you may not download an entire issue of a journal or multiple copies of articles, and you may use content in the JSTOR archive only for your personal, non-commercial use. Please contact the publisher regarding any further use of this work. Publisher contact information may be obtained at http://www.jstor.org/action/showPublisher?publisherCode=esa. Each copy of any part of a JSTOR transmission must contain the same copyright notice that appears on the screen or printed page of such transmission. JSTOR is a not-for-profit organization founded in 1995 to build trusted digital archives for scholarship. We work with the scholarly community to preserve their work and the materials they rely upon, and to build a common research platform that promotes the discovery and use of these resources. For more information about JSTOR, please contact [email protected]. Ecological Society of America is collaborating with JSTOR to digitize, preserve and extend access to Ecology. http://www.jstor.org Ecology, 87(8), 2006, pp. 1915-1924 ? 2006 by the the Ecological Society of America HABITAT LOSS, TROPHIC COLLAPSE, AND THE DECLINE OF ECOSYSTEM SERVICES Andrew Hal David Dobson,1'10 Jackie Lodge,2 A. James Mooney,6 Graeme Alder,3 Osvaldo Rusak,2'11 S. Cumming,4 Volkmar Sala,7 and Marguerite A. Wolters,8 Juan Keymer,1 Diana Wall,9 Jacquie McGlade,5 Rachel Winfree,1 Xenopoulos2'12 1 Department Princeton New Jersey 08544-1003 and Evolutionary USA Princeton, University, of Ecology Biology, Sciences, of Biological University of Notre Dame, P.O. Box 369, Juniper and Krause Streets, Notre Dame, Indiana 46556-0369 USA V6T 1Z4 Canada The University British Columbia 3Fisheries Centre, 2204 Main Mall, Vancouver, of British Columbia, Institute of African Ornithology, 7701, Cape Town, South Africa of Cape Town, P. Bag Rondebosch University 4[Percy FitzPatrick 5 10 The Coach House, University College Compton Verney CV35 9HJ UK of London, 94305-5020 USA Sciences, Stanford University, Herrin Labs, Room 459, Stanford, California of Biological 6Department Brown University, and Evolutionary Rhode Island 02912 USA Providence, of Ecology Biology, 7Department Giessen, Germany of Animal Ecology, Justus-Liebig-University of Giessen, Heinrich-Buff Ring 26-32 (IFZ), D-35392 8Department State University, Fort Collins, Colorado USA Colorado 80523-1499 9Natural Resource Ecology Laboratory, 2Department Abstract. of sustaining and services that we provisioning goods for the conservation of economic strong justification these the relationship between and services and goods The is a ecosystems Understanding and arrangement, In management. habitats of natural is a fundamental quality we describe a new this paper, approach changes of natural challenge to from obtain biological the assessing natural diversity. in the size, resource of implications loss for loss of ecosystem services by examining how the provision of different ecosystem services is dominated by species from different trophic levels. We then develop a mathematical model that illustrates how declines in habitat quality and quantity lead to sequential losses of trophic diversity. The model suggests that declines in the provisioning of services will initially be slow but will then accelerate as species from higher trophic levels are habitat lost at rates. faster collapse (and these patterns similar suggest In general, change. anthropogenic of Comparison assembly) ecosystem with empirical in natural occur patterns and goods services of examples systems by provided ecosystem impacted species by in the upper trophic levels will be lost before those provided by species lower in the food chain. The decrease in terrestrial food chain length predicted by the model parallels that observed in the oceans following as them susceptible Whereas exploited. extinct by on the this trophic as traditional order-of-magnitude loss of an entire the represent species an The overexploitation. to extinction area large are they species-area in habitat decline trophic level and conservation; ecosystem Key biodiversity; Lake; species-area; species loss; trophic collapse. Introduction The study of of goods and from theoreticians predict the effects ecosystems services has and that decreases and attracted all this magnitude of services performed abundance, the ecosystem loss may by the level. words: functioning of higher levels make trophic where they are systematically are driven that 50% of species requirements in marine systems curve suggests in ecosystem reductions of biodiversity their much experimentalists. in biodiversity on the to provide ability recent attention Ecologists will lead to received 31 December 13 January 2004; revised Manuscript 16 January 2006. Corresponding Editor: R. B. 2006; accepted see footnote Jackson. For reprints of this Special Feature, 1, p. 1875. 10 E-mail: [email protected] 11 Present Center for Limnology, address: of University Trout Lake Station, Wisconsin-Madison, Boulder-Junction, Wisconsin 54512 USA. 12 Present address: Department of Biology, Trent Univer K91 7B8 Canada. Ontario, sity, Peterborough, of provisioning web; Little services; food ecosystem function; Rock in the and hence functioning et al. 1994, 1995, Daily et al. 2000, Loreau 2000, Chapin services (Naeem et al. 1997, 1997, Daily et al. 2001). The exact shape of this relationship depends on the ecosystem as well as the order and service process in which species are lost or potentially from, added to, the ecosystem (Mikkelson 1993, Sala et al. 1996, Petchey et al. 1999, Petchey and Gaston 2002, Duffy 2003). A number of possible functional have forms been sug that couple biological gested for the relationships diversity to the rate and resilience with which different types of are undertaken processes ecosystem 1996, Tilman et al. 1996, Kinzig all of these maximum declines 1915 is the argument rate to zero at which as species that the (Sala et al. et al. 2001). Central to there activity diversity is some asymptotic is undertaken that and abundance are 1916 ANDREW ET AL. DOBSON 40 in Primary producers 20 these be may almost under land 1986 The 1987 earliest linearly each of stage 8 water and the upon dependent habitat conversion diversity-functioning -40 Large-scale ground the explicitly investigate on focused above relationship and plant production species diversity. primary manipulative species in different -60 pattern, with decreases in similar Tertiary consumers small -80 ?CO 20 no discernible -60 services and -80 becoming a! -120 habitats et al. (1993) and reduced (Mikkelson et al. Crawley one only for (B) in Schindler 1993, Tilman 1999, or a few Loreau species Examples studies show lost ecosystem levels different trophic are studies from the species more rapidly of services as uses. marine levels higher trophic from than species are lower loss of habitat quality or quantity and services are in a predictable ecosystem ecosystem sequence and terrestrial, at slowly et al. Larsen 2002, on other is types needed freshwater, that These levels species, or on loss biodiversity ecosystem et al. (Kremen habitat particularly relating algal production other trophic levels with \-$). of of ecosystem replacement or converted for other disrupted are Stres specific loss in primary of effects for -100 (Figs. examine in rates (Schindler et al. 1985). Empirical available typically that in little changes the but more 2005), or the collapse Brezonik further in decreases resulted diversity experiments resulted acidification of carnivorous (initial N =9 (B) primarily Zooplankton species). consumers in Lake 223, Ontario, Canada Quaternary (initial N = 7 fish = = 5.59, final pH 4.75; for species). For (A), initial pH = = 5.13. fish data were 6.49, final pH (B) initial pH Complete taxa were unavailable for (A), and complete data for other unavailable for (B). For of recruitment (B), the cessation was treated as species extirpa (absence of young-of-the-year) are available tion. Additional details for (A) in experimental production in resulting while (Tilman et al. 1996, 1997, Hector et al. 1999). evidence loss (as a percentage of pre species to gradual in response number) experi in two north lakes. (A) Four temperate in Little Rock USA: Lake, Wisconsin, = 51 primary (initial N producers phytoplankton species); consumers TV= 36 primarily herbivorous primary (initial = 9 consumers secondary (initial N Zooplankton species); consumers omnivorous and tertiary Zooplankton species); losses species primary species decomposition 1. Annual acidification species mental acidification levels lower-trophic all showed a production and Fig. the first grassland using in sors, 1977 CD -20 O) cc i?? c -40 CD experiments regions of the world reductions In whole-lake 0 to experiments -20 where nutrients of 87, No. (Dobson 2005). 0 1998, amount the cases, processed area of Vol. Ecology, other examples dominated way. services A by logical respond that suggest specific inference some trophic is that to loss of differently if the spectrum of functional forms services (producers to biodiversity onto maps to consumers). Thus we might et al. (1985). et al. 1997, Loreau et al. undertake In cases 2001). the ecosystem function then decline may be rapid as the abundance of the activity declines the species undertaking (for of herbivores top by regulation are functions of this ecosystem type as brittle. In contrast, classified there will be other types a function where between of ecosystem competition example, population carnivores); diversity so that by of species may loss of one the in increase the create species abundance considerable may be and 0.08 redundancy, for compensated activities of a similar that occupies niche (Naeem competing species rate at which In these the relative and Li cases, 1997). as species slow will be relatively the process declines we would For example, decline. and abundance diversity argue cleansing compete that this where with is the case for nutrient and water cycling a huge of microbial diversity species each other while the function; undertaking a 0.06 Perimeter-to-area 0.04 0.02 ratio 2. Fig. of landscape simplification (decreasing Impact of loss (as percentage ratio) on the species perimeter-to-area of herbaceous species number) (line a) pre-acidification plants and carabid fields trophic groups (lines b-d) inhabiting wheat = located in central Germany groups of carabids 35). Trophic (n include (b) mixophagous, and (d) predaceous (c) phytophagous, are (c) 40.3 (P < 0.05) and coefficients species. The regression the slopes of (a) and (P < 0.005); (d) 66.3 (b) are not different from zero (Purtauf et al. 2005.). significantly DETERMINANTS OF BIODIVERSITY CHANGE 1917 August 2006 100 few Primary producers o Primary consumers Secondary consumers Q. O TO 10 T 6> O T .C pattern O "cO C/) with V 10 on each no. species Total 100 3. scatter to the data, the rate of there is considerable Although decline of plant species (solid circles) has a shallower slope than consumers the rate of decline of primary (open circles). The consumers et al. show no clear pattern, but Terborgh secondary on the smaller in ant abundance (2001) record huge increases islands in terminal stages of collapse, on ants has essentially disappeared. brittle such as carbon services; of provisioning that depend are chains also aim is consider under the diversity thus levels, we that also may these quantity; recreation, the services services collapse by assuming We recognize that in habitat to relationships loss. Second, we on 2000), forms key but explicitly ecosystem assumes that predominantly then model ecosystem is lost. trophic that their such the similarly services associated activity of (Bunker et empirical many provided al. example 2005). The would Naeem processes predominantly located at specific species most be that most Such services levels, loss an be drugs, and genetic on readily these "type C" as each from species characteristics unique for compensated loss the essence, of each in the loss of a "unit" of of Examples the provisioning include in service depend with In species results the biodiversity intermediate, may cannot they prey. are responses fall between decrease each species. of would example, a linear E type service. ecosystem of resources, C type fruits, ecosystem pharmaceut supporting CO .<D 500 ? CD ?" 400 services J 3001 - ?All species -o- Plants - Plants and herbivores 200i 100 result processes regulation; ecosystem result and trophic include species the abundance regulation levels on which A we diversity-service such by relationships remaining individual species lower levels. ecosystem of population species. services, at of trophic and show would species by and brittle brittle very type For multiple these more provided lower service extremes. 1880 from the interaction between trophic levels (particularly many services of mapping trophic most are fragile 600 that higher trophic levels decline lower than rapidly We levels. trophic specific are in in the First, between and reduction species-area or the 700 explored manuscript). to biodiversity decline ecosystem specific more use be are changes These rare keystone ecotourism, species response ical trophic when relationship a simple, but plausible, onto which biodiversity, propose explicitly will unpublished possible we essentially link habitat model complications in species diversity decline by is no lost, the on have Services relationships. services on different species increase in prey abundance (A. P. Dobson, the simplest assume and between there are predators elsewhere The is a there trophic diversity services. ecosystem interactions ignores of biodiver that assumption between simple mapping of the consequences na?ve services. to supply likely acknowledge levels two habitat further the relationships evaluate between we have and ecosystem services, trophic collapse, a three of built model component phenomenological loss decline of Our and services. ecosystem biodiversity small in large changes ecosystem or and control, responses services, fuel While many species located in the upper levels of trophic ecosystem To E type these result that recognize conditions boundary loss of ecosystem erosion storage, predominantly loss, principal loss sity for services; of provisioning with total biomass In contrast, protection. We to see a predictable hierarchical as habitats are eroded. expect services most of that pr?dation implying cover species biodiversity island loss and net species diversity (log-log scale) Species on different et al. islands in Lago Guri (after Terborgh on is more advanced 1997a, b, 2001). Ecological collapse lower net smaller islands with species diversity (x-axis). Fig. plant storm this as such primary production or associated and fiber, wood 0.1 that be those directly associated these will be predominantly -i' g> o CD Q. en et al. 2003.). We suggest as type A ecosystem loss be classified 1999, Vinebrooke of in a result et al. (Schindler et al. 1995, Crawley 1995, Frost 1994, losses species services of a losses the remaining for by compensated et al. 1985, Naeem where studies further eventually in ecosystem decrease et al. 8 CD are mostly species until species drastic O in grassland observed response 0 the their from the levels observed primary-production 1920 1940 1960 1980 Year et al. and trophic commonly 1900 on Krakatau Fig. 4. Recovery of trophic diversity follow that led to the total extinction of all ing the volcanic eruption life on the island lowest line (after Thornton 1996). The illustrates the number of plant species on the island, the middle line is the number of herbivore of predatory species. number species, and the top line is the 1918 ANDREW as such pollination provision istics play et (Kremen nutrient 2003), cycling al. of habitat where a unique ecological individual role et Klein 2002, et al. 2000), (Schwartz al. and character species' as pollinators or seed dispersers (Kremen 2005). We have used the list of ecosystem and goods services developed by theMillennium Ecosystem Assessment as the basis of our list of services provided by different and natural Millennium from the to biodiver services consensus represent after in services were services table discussions classified ently in the each author each ecosystem. to be Some consistently thought services ecosystems (primary production), were more in some others considerably fragile tems in others As we than control). (biological took it became this exercise, ecosystem strongly to services on dependent that changes in of sufficient the biodiversity-service ple, provisioning relationship. is the dominant of food cultivated lands, which is a production, and shows a type A forest the ecosystems, dominant service but productivity response. of provisioning is not directly and to rather the the under type further exam in is not the of presence to primary a broader spectrum of species (from fungi to plants and animals); it has a type C the dominant whereas service, response, to has a type A response. of fiber, Sensitivity loss was minimal for services predominantly provision biodiversity provided by decomposers and primary producers (type A) and maximal in the case of services provided by top predators (type E). The general patterns described in Table might services two 1 identify construct as a key that we any model in changes habitat increasing of result for assumptions predicts of faunal support are collapse will ecosystem Lambert increase of collapse et al. 2003); in herbivores the (Terborgh are these when trophic levels go extinct. This overexploitation of plant of events sequence species, et al. our predators by massive at higher in turn is followed so that to lead 1997?, b, 2001, characterized the that lost as pattern holds will 50 after the restructure were years there to colonize. the net in size, by the vegetation becomes dominated by inedible and thorny species. This we here that decline will in the at many species area larger requirements rate at lower than those faster lake acidification and (Menge cally more fewer resting 1987). For levels trophic they are physiologi environmental to survive stages higher same the Sutherland because to habitat quality example, ecosystems, susceptible this modify because have a at in aquatic example, unfavorable stress, have periods, and are more dispersal limited (Menge and Sutherland 1987, Bilton et al. 2001, Vinebrooke et al. 2003). An increasing body of evidence suggests that species at higher trophic levels have steeper in their slopes relation species-area ships (Holt et al. 1999), and that food chain length is a function of habitat size and Newman (Cohen Post 1991, et al. 2000, Post 2002). A combination of such theoretical and empirical studies suggest that declines in either habitat quantity (or quality) leads to decreases of food chains and thus a more loss lengths rapid at higher services levels. by species provided trophic in the the Modeling These Ecosystem us allow services ecosystem series of Decline observations of collapse hierarchical of nested to will Services that suggest be determined the a by or breakpoints, thresholds, whose magnitude will occur at different levels of decline we snapshots that on Krakatau ecosystems only will levels declines, in overall trophic and relationship; assume trophic be more rapidly than those at lower trophic levels (Figs. 1 4; Wardle et al. 1997, Terborgh et al. 2001, Kremen 2005, Larsen et al. 2005). The classic studies of John Terborgh and colleagues on the islands of Lago Gur? levels webs and and lost illustrate at higher a sequential lower levels note recovery trophic levels (Holt et al. 1999). When (1) species at different trophic levels perform different ecosystem services and (2) species at higher trophic levels will be lost more rapidly than those at lower levels. trophic A number of examples contention that species higher of ecosystem losses: a final decline disproportionately In contrast, related successively we example, for predators are eroded habitats natural approach they service of food seen that has to top resources species-area to primary related service food structure the ecosystem herbivores, As is For ants. in species diversity has traditionally been described by a under sensitivity service that they provide that then ecosystem in decomposing In marine systems, increase of surveys suggest ecosys service each a change in food web from loss of species of the food web. As while of an by leaf-cutter 8 fishing has explicitly focused on the removal of species from higher trophic levels this "fishing down of the food chain" has led to a shortening of the food chain. In contrast, in the Little Rock lake food web example (Locke 1996), acidification of the water supply has led to across biodiversity the ecosystem species providing consideration. Characteristics modify the location the trophic dominant and the dominant apparent is matched particularly 87, No. themselves from the bottom up (Thornton et al. 1988, Thornton 1996); the island was first colonized by plants, independ resilient turn in species, Vol. Ecology, long-term that all of 1; (Table 2003). We have then of ecosystem response Values change. emerged ecosystems Ecosystem Assessment the classified sity human-modified ET AL. DOBSON effect, web in a way In abundance. species assume that we can that the most such rank to model order the species resilient this in a food species are at the bottom of the food chain, while the least resilient are at the top of food chain. Itmay be that body size is a key of determinant however, ity; some are much pathogens both there are are tiny, trophic position resilience, to this general important exceptions such as elephants and whales key herbivores in contrast than their larger predators, but are key regulatory at all trophic levels. Empirical relationship and between body components studies supporting size, trophic level, the and 1919 DETERMINANTS OF BIODIVERSITY CHANGE 2006 August assessment 1. Qualitative ecosystems. Table of of different the susceptibility Urban service Provisioning Fresh water Fiber Fuel wood Food resources Genetic and Biochem Cultivated A A A A NA NA pharmaceuticals resources Ornamental Drylands of different type Ecosystem Ecosystem loss for a number to species functions ecosystem Inland water Forests and woodlands Coastal Mountain Island systems Polar Marine E A E A E A A A A A C C A A A C C c NA A E A E E C E NA E C C A A A A C C ? A A A C C A E E E C E NA A E E C E A A A A A A A A A B A A A C B A A E E E A A E C A A A A A C A A A A C A A A A A A A NA NA A NA Regulating Air quality Climate regulation control Erosion Storm protection Water purification treatment and waste of human Regulation diseases Detoxification control Biological Cultural Cultural and diversity B C C A C D A E C D C D E E A E C c C c E A A E A D D C E E E C C D A D D C E E E C C A A A A A A A A A A A A A A E A A A A A A A A A A A A A A NA C C D E E E C C C C C c A C E NA A D C C C C C c E E A NA A E C D identity Recreation and ecotourism Supporting Primary production 02 production Soil formation and retention Pollination Nutrient cycling Provision of habitat Notes: losses of a few species are mostly for by the remaining services are those for which Type A ecosystem compensated to species loss, with Type E representing services that depend primarily on rare susceptible species. Types B-E are successively more or fragile species (see Introduction). "?" indicates not known. "NA" indicates not applicable; diversity have been achieved following intense and painstaking field studies of a limited number of food webs (Briand and Cohen 1987, Schoener 1989, Cohen et al. These 2003). general insights of estimates Our to that we of services the (A), primary of Alternatively, approximate of relative at which on declines this we need explicit decomposers auto (Z>), (P), and secondary of well-studied food webs. estimates of the relative numbers of each of these species (Briand and Cohen 1984, Cohen 1989, Schoener 1989). Here, we have opted successive diversity conclusions invariance. to assume a levels. We trophic on successive are We robust then constant have ratio of at 4:3. levels trophic to this na?ve assumption obtain an species set the ratio estimate of of species main Our of total on scale species of estimate exhaustively will particularly at We the diversity ratio-based an obtain the total we explicitly acknowledge need. consumers in a variety (Q we can use consumers as breakdown numbers number initial the thresholds level. To achieve of sufficient calibrate coarsely magnitude each trophic trophs is step hierarchical estimates us the parameters first ecosystem a provide to provide studies for diversity by summing the totals for each trophic level to then services total to provided number set by of trophic the by species (here "threshold" as either will We species total diversity, levels). decomposers species. between characterized to underestimate lowest need relationship be lead us the of number that our inability to sample for decline a fraction assume and the that function diversity an asymptotic of of or the can S-shaped function and that this function can be characterized by a level of diversity at which the function operates at 50% of its theoretical maximum. For any trophic level, we will assume that this threshol4 level of diversity is determined when the total number of species has been reduced to some fraction p of their original diversity. The fraction unity (as p ? trophic this level), could take any value between zero and 0, the services become more brittle at any we will set this value to 0.1, and argue that the log-normal reflects distri phenomenologically of species bution abundance within each level trophic 1920 ANDREW DOBSON ET AL. 0.4 Species Vol. Ecology, 0.6 8 87, No. 1.0 composition Fig. 5. Functional forms for the relationship loss of biodiversity between and loss of function. Each of the curves represents the in both number of species at each trophic level and the ecosystem decline services undertaken by species on different trophic levels as the total number of species in the community declines. The lowest line (alternating is for predators dots and dashes) and services on the top trophic level, the second lowest line is for herbivores, the dotted line is for plants, and the solid line is for decomposers. The threshold values occur when each trophic level passes the value of species composition that corresponds to 50% of through maximum for services efficiency a major to the commonly than 90% of the contribution that phenomenon greater level. of relative abundance 1975). This distribution (May makes at that trophic undertaken observed ecosystem functioning is undertaken by less than 10% of the species (at any trophic level; Tilman et al. 1997, Loreau 1998, Petchey and Gaston 2002). can We now set sequentially the breakpoints for growth changes with increasing population density (Maynard Smith and Slatkin 1973, Bellows 1981). This simple function builds upon the hierarchical thresholds and above developed and the upper more levels brittle. with Rx at p X D. abundance left has in the assumes This so declined that then community, only services species are species p X D performed the by lowest trophic level will have declined by 50%. The (50%) threshold for the next trophic level (autotrophs) is set for when species diversity is reduced to D + p X A assumes This species. that at processes the second same as at constant proportionality (although we could readily modify even more levels trophic we data empirical will brittle; maintain of constant p). The assumption set thresholds and for primary the lower level this to make upper of more in the absence We level now define ecosystem to community. was that the net Here originally a function parsimonious same us logic allows consumers secondary that relates are performed number of species a modified we use developed the at each to strength with which density dependence by on species species ecosystem level x, S trophic in the degraded surviving services are is the total and habitat, Tx is the threshold level of diversity calculated above for x. Note level trophic assumed that species determined x parameter that are by to we here lost from we RT, characterize each use the have intrinsically level at a trophic the trophic-level with steepness which services (and species) are lost as diversity declines, and we have set arbitrarily, level. The trophic this way in species declines as function with which a square of this function and diversity ecosystem rate Standard curves species-area may be to mimic used the net loss of biodiversity as habitat is either lost or declines in quality (Simberloff 1988, Reid 1992). We at note trophic in the remaining of a function characterize performed number of at which at form to RT rate the function at different trophic levels is illustrated in Fig. 5. our more services Here, is characterizes D + A + p X P and D + A + P + p X C, respectively. which '< rate trophic level will decline at an earlier level of species loss than that at which the basal level declines. We use the (i) \ set the net that when species 1 = the threshold (50% efficiency) level for the lowest trophic level in which way decreasing each we Thus decline diversity: trophic level in a way that will give a hierarchical series of breakpoints with the lowest trophic levels being most resilient a general describes services ecosystem the in population that X number, assumes brium. the = that the A number species-area than function continental curves N z = area, = cXz slope, (where c = and = N a comes community rapidly of studies that the have shown tends scales and to b? steeper on that slopes are species constant), to equili local also slope of rather steeper DETERMINANTS OF BIODIVERSITY CHANGE 1921 August 2006 a more rate rapid lower those than by provided at species levels. trophic It is also possible to use Eq. 1 (and its underlying trophic thresholds) to calculate food chain length at different stages of habitat decline (Fig. 6B). This allows with comparison of studies marine freshwater and systems where decrease in food chain length in response to overexploitation is indicative of declines in "ecosys tem size and an al. et Post 1998, al. to a loss in habitat leads of magnitude only a in species this number, represents to an structure in community equivalent order 50% et (Pauly quality" important observation here is that, although 2000). An reduction change average one position of in the average level decline trophic the species persisting in the trophic A community. second order of magnitude decline in habitat causes the loss of the top trophic level from the remaining a matches This community. exploited marine causes overexploitation Our positions. result in heavily observed (Pauly et al. fisheries a decline in an adds approach 1998), where average trophic important detail: trophic collapse would seem to be initiated by first a thinning of the species throughout the web (which 0.001 0.0001 would 1 0.1 0.01 Proportion of habitat remaining in abundance of species from different (A) Decline is lost at a constant levels as habitat annual rate. The trophic solid black line illustrates the net loss of species as habitat lines reflect loss of species and, hence, declines, while the broken services from sequentially lower trophic levels. The ecosystem line represents the alternating lowest dashed top consumers, Fig. the produce in mean decline observed 6. are to variation in the slope of the species-area to significant in robust variations relatively of the model: the two other ratio parameters principal on and of species levels, diversity sequential trophic robust curve and at rates in inequality which drive species the middle dashed line dotted-dashed line is primary consumers, is plants and the dotted line is decom (primary producers), between posers (B) Relationship (bacteria and soil organisms). area of habitat remaining and length of food chain. The dashed processes (characterized by p). We would the maximum possible length of the food chain in the the solid line shows the total proportion of habitat, remaining and the dotted line illustrates the original species still persisting, of the surviving average species. trophic position by line shows see an and initial a more rapid This services. for real islands than for habitat islands (Scott et al. 1998).We will assume that loss of diversity on a local be may characterized a by z = slope 0.33 1967, Connor and McCoy (MacArthur and Wilson This Simberloff 1979, 1992). slope leads to a 50% decline in net species diversity for each order of magnitude decline area. in habitat to normalize ward loss species level as the species a proportional be used relatively to curve and express loss from each trophic habitat the characterize straightfor-. area to proportional in response then It is then loss loss. of Eq. 1 can ecosystem functioning from each trophic level as habitat is either lost or degrades in quality (Fig. 6). The model illustrates that although the overall is comparatively trophic levels modest, are lost most loss of because rapidly, species species as area at declines the highest the economic goods and services provided by these species will thus be lost at implies are systems these of of collapse sequential the sequence that declines the relative Determining which services breakdown tween be may similar in different on different requires further species thresholds ecosystem and that the and predictable of the how (Table 1). at thresholds interactions be affect these levels trophic and goods of ecosystems position and goods followed degraded, service loss is likely to be hierarchical sequence ecosystem thus expect to in economic reduction sequential as natural services potentially scale trophic position), followed by a more rapid shortening of the food web (the loss of top trophic levels). These results attention. urgent Conclusions model The between therefore the upper diversity levels are interactions such predators Terborgh by plants ignored modified key are ignored thus prey release) as levels ecological abundance by (Terborgh and maintenance in this It will in abun important of regulation interaction levels. changes intermediate at species removed, as 1997&), framework. of soil We 1988, structure have also the fact that many habitats are explicitly to create new habitats that directly supply to services agriculture, of no trophic compensatory (meso-predator et al. assumes here at different underestimate and dance described species but the also human lands economy, for industry, particularly homes, and ANDREW 1922 ET AL. DOBSON 87, No. Vol. Ecology, 8 If services as top predators. 1. Both lions and tigers provide Plate They also act as a major draw for ecotourists. ecosystem such as these, it is likely that they will also of top predators reserves can maintain and nature healthy populations ecosystems of ecosystem services at lower trophic of the many and populations contain healthy communities species that perform a diversity levels. Photo credit: A. P. Dobson. recreation. Some models in that explicitly explore changes under services ecosystems are conversion habitat described in Dobson (Dobson 2005). Similarly, the model ignores the impact that alien species might have when they replace and compete with those left in a degraded community. This will be particularly impor tant in agricultural are habitat natural The service. ecological large portions into monocultures that level) phototrophic where areas, converted of relevance area curves to rates estimate of the loss of biodiversity Bevers 2002). biodiversity for local accurate Consequently, of estimation loss has to take into account the potential as extinctions not arrangement, a as just consequence a of function of habitat net habitat remaining. The model framework we have developed could be adapted to consider all of these processes, the to a first approximation, modifying although magnitude of the threshold parameters (/?,-)may most subtle readily capture the details of these more processes. None because of this detracts from our principal conclusion; services ecosystem to be tend to top we bottom, hierarchical predictable economic earthworms, goods they become and would and services expect sequential by natural fungi, crucial the economically water but as nematodes, such species undertake and bacteria many In contrast, species. not also food structure only and the energy chain and by that nutrients and primary At attention. conservation buffering air and that cleanse processes limited receive (plants) provide against are then secondary but erosion, up passed consumers. the The empirical examples and phenomenological model described above suggest that the ecosystem services undertaken by species at high trophic levels will disappear before those undertaken by species at the bottom of the food chain. While the economic effects of this loss in services have so far been limited, the loss of species that benefit by simply serving aesthetic and (see Plate services recreational as an 1), serves important alarm bell for the subsequent loss of services to which human health and economic welfare are more tightly because Ironically, coupled. the volume of essential services provided by species at lower trophic levels is linearly dependent upon the size (and quality) of habitat the remaining, essential services viable best way may for be species to maximize to ensure with larger return that area the on these ecosystem requirements that have less readily quantified economic value. under taken by species at different trophic levels and because trophic webs will tend first to thin and then collapse from these remains different carnivores top intermediate trophic levels, autotrophs (Simberloff 1988, Seabloom et al. 2002). Although habitat amount is of primary importance in determining the size and ultimately the persistence of populations, the spatial arrangement of persisting habitat patches becomes increasingly more important as habitat is lost (Flather and Bevers 2002). There is a rapid*decline in connectivity once 30-50% of habitat is lost, which may have a significant impact on population dynamics and interactions between species (Cumming 2002, Flather and to conserve time the present such as tigers, wolves, and fish (species that provide a heightened spiritual and recreational quality to ecosys tems), there is limited economic incentive to conserve of in using species at pressure mites, pattern spatial remains one of the central problems the (at as a major food supply of activities. This apparently simple, but important, insight has been overlooked in previous studies of ecosystem there is significant conservation functioning. 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