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The relationship between species richness and productivity in metazoan parasite communities

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Abstract

Biodiversity is not distributed homogeneously in space, and it often covaries with productivity. The shape of the relationship between diversity and productivity, however, varies from a monotonic linear increase to a hump-shaped curve with maximum diversity values corresponding to intermediate productivity. The system studied and the spatial scale of study may affect this relationship. Parasite communities are useful models to test the productivity-diversity relationship because they consist of species belonging to a restricted set of higher taxa common to all host species. Using total parasite biovolume per host individual as a surrogate for community productivity, we tested the relationship between productivity and species richness among assemblages of metazoan parasites in 131 vertebrate host species. Across all host species, we found a linear relationship between total parasite biovolume and parasite species richness, with no trace of a hump-shaped curve. This result remained after corrections for the potential confounding effect of the number of host individuals examined per host species, host body mass, and phylogenetic relationships among host species. Although weaker, the linear relationship remained when the analyses were performed within the five vertebrate groups (fish, amphibians, reptiles, mammals and birds) instead of across all host species. These findings agree with the classic isolationist-interactive continuum of parasite communities that has become widely accepted in parasite ecology. They also suggest that parasite communities are not saturated with species, and that the addition of new species will result in increased total parasite biovolume per host. If the number of parasite species exploiting a host population is not regulated by processes arising from within the parasite community, external factors such as host characteristics may be the main determinants of parasite diversity.

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References

  • Abrams PA (1995) Monotonic or unimodal diversity-productivity gradients: what does competition theory predict? Ecology 76:2019–2027

    Google Scholar 

  • Bargelloni L, Marcato S, Zane L, Patarnello T (2000) Mitochondrial phylogeny of notothenioids: a molecular approach to Antarctic fish evolution and biogeography. Syst Biol 49:114–129

    CAS  PubMed  Google Scholar 

  • Bininda-Emonds ORP, Gittleman JL, Purvis A (1999) Building large trees by combining phylogenetic information: a complete phylogeny of the extant Carnivora (Mammalia). Biol Rev 74:143–175

    CAS  Google Scholar 

  • Bonine KE, Garland T Jr (1999) Sprint performance of phrynosomatid lizards, measured on a high-speed treadmill, correlates with hindlimb length. J Zool 248:255–265

    Article  Google Scholar 

  • Butler MA, Losos JB (1997) Testing for unequal amounts of evolution in a continuous character on different branches of a phylogenetic tree using linear and squared-change parsimony: an example using lesser Antillean Anolis lizards. Evolution 51:1623–1635

    Google Scholar 

  • Chase JM, Leibold MA (2002) Spatial scale dictates the productivity-biodiversity relationship. Nature 416:427–430

    Article  CAS  PubMed  Google Scholar 

  • Choudhury A, Dick TA (2000) Richness and diversity of helminth communities in tropical freshwater fishes: empirical evidence. J Biogeogr 27:935–956

    Article  Google Scholar 

  • Connell JH (1978) Diversity in tropical rain forests and coral reefs. Science 199:1302–1310

    Google Scholar 

  • Cornell HV, Lawton JH (1992) Species interactions, local and regional processes, and limits to the richness of ecological communities: a theoretical perspective. J Anim Ecol 61:1-12

    Google Scholar 

  • DeBry RW, Sagel RM (2001) Phylogeny of Rodentia (Mammalia) inferred from the nuclear-encoded gene IRBP. Mol Phyl Evol 19:290–301

    Article  CAS  Google Scholar 

  • Densmore LD, Rose FL, Kain SJ (1992) Mitochondrial DNA evolution and speciation in water snakes (genus Nerodia) with special reference to Nerodia harteri. Herpetologica 48:60–68

    Google Scholar 

  • Dobson AP (1985) The population dynamics of competition between parasites. Parasitology 91:317–347

    PubMed  Google Scholar 

  • Dodson SI, Arnott SE, Cottingham KL (2000) The relationship in lake communities between primary productivity and species richness. Ecology 81:2662–2679

    Google Scholar 

  • Estes R, de Queiroz K, Gauthier JA (1988) Phylogenetic relationships within Squamata. In: Estes R, Pregill G (eds) Phylogenetic relationships of the lizard families. Stanford University Press, Stanford, Calif., pp 119–281

  • Felsenstein J (1985) Phylogenies and the comparative method. Am Nat 125:1-15

    Article  Google Scholar 

  • Garland T Jr, Harvey PH, Ives AR (1992) Procedures for the analysis of comparative data using phylogenetically independent contrasts. Syst Biol 41:18–32

    Google Scholar 

  • Giannasi N, Thorpe RS, Malhotra A (2000) A phylogenetic analysis of body size evolution in the Anolis roquet group (Sauria: Iguanidae): character displacement or size assortment? Mol Ecol 9:193–202

    Google Scholar 

  • Grace JB (1999) The factors controlling species density in herbaceous plant communities: an assessment. Perspect Plant Ecol Evol Syst 2:1–28

    Google Scholar 

  • Graybeal A (1997) Phylogenetic relationships of bufonid frogs and tests of alternate macroevolutionary hypotheses characterizing their radiation. Zool J Linn Soc 119:297–338

    Article  Google Scholar 

  • Gregory RD (1990) Parasites and host geographic range as illustrated by waterfowl. Funct Ecol 4:645–654

    Google Scholar 

  • Grime JP (1973) Competitive exclusion in herbaceous vegetation. Nature 242:344–347

    Google Scholar 

  • Harvey PH, Pagel MD (1991) The comparative method in evolutionary biology. Oxford University Press, Oxford

  • Hillis DM, Davis SK (1986) Evolution of ribosomal DNA: fifty million years of recorded history in the frog genus Rana. Evolution 40:1275–1288

    CAS  Google Scholar 

  • Holmes JC, Price PW (1986) Communities of parasites. In: Anderson DJ, Kikkawa J (eds) Community ecology: pattern and process. Blackwell, Oxford, pp 187–213

  • Huston MA (1979) A general hypothesis of species diversity. Am Nat 113:81–101

    Article  Google Scholar 

  • Huston MA, DeAngelis DL (1994) Competition and coexistence: the effects of resource transport and supply rates. Am Nat 144:954–977

    Article  Google Scholar 

  • Jackman TR, Larson A, de Queiroz K, Losos JB (1999) Phylogenetic relationships and tempo of early diversification in Anolis lizards. Syst Biol 48:254–285

    Article  Google Scholar 

  • Jones KE, Purvis A, MacLarnon A, Bininda-Emonds ORP, Simmons NB (2002) A phylogenetic supertree of the bats (Mammalia: Chiroptera). Biol Rev 77:223–259

    Article  Google Scholar 

  • Kennedy CR, Guégan J-F (1996) The number of niches in intestinal helminth communities of Anguilla anguilla: are there enough spaces for parasites? Parasitology 113:293–302

    Google Scholar 

  • Lauder GV, Liem KF (1983) The evolution and interrelationships of the Actinopterygian fishes. Bull Harvard Mus Comp Zool 150:95–197

    Google Scholar 

  • Leibold MA (1999) Biodiversity and nutrient enrichment in pond plankton communities. Evol Ecol Res 1:73–95

    Google Scholar 

  • Loreau M, Hector A (2001) Partitioning selection and complementarity in biodiversity experiments. Nature 412:72–76

    CAS  PubMed  Google Scholar 

  • Mackey RL, Currie DJ (2000) A re-examination of the expected effects of disturbance on diversity. Oikos 88: 483–493

    Google Scholar 

  • Mackey RL, Currie DJ (2001) The diversity-disturbance relationship: is it generally strong and peaked? Ecology 82:3479–3492

    Google Scholar 

  • Mitchell-Olds T, Shaw RG (1987) Regression analysis of natural selection: statistical inference and biological interpretation. Evolution 41:1149–1161

    Google Scholar 

  • Mittelbach GG, Steiner CF, Scheiner SM, Gross KL, Reynolds HL, Waide RB, Willig MR, Dodson SI, Gough L (2001) What is the observed relationship between species richness and productivity? Ecology 82:2381–2396

    Google Scholar 

  • Morand S (2000) Wormy world: comparative tests of theoretical hypotheses on parasite species richness. In: Poulin R, Morand S, Skorping A (eds) Evolutionary biology of host-parasite relationships: theory meets reality. Elsevier, Amsterdam, pp 63–79

  • Morand S, Poulin R (1998) Density, body mass and parasite species richness of terrestrial mammals. Evol Ecol 12:717–727

    Article  Google Scholar 

  • Murphy WJ, Eizirik E, Johnson WE, Zhang YP, Ryder OA, O'Brien SJ (2001) Molecular phylogenetics and the origins of placental mammals. Nature 409:614–618

    Article  CAS  PubMed  Google Scholar 

  • Nelson JS (1994) Fishes of the world, 3rd edn. Wiley, New York

  • Oba G, Vetaas OR, Stenseth NC (2001) Relationships between biomass and plant species richness in arid-zone grazing lands. J Appl Ecol 38:836–845

    Article  Google Scholar 

  • Poulin R (1995) Phylogeny, ecology, and the richness of parasite communities in vertebrates. Ecol Monogr 65:283–302

    Google Scholar 

  • Poulin R (1997) Species richness of parasite assemblages: evolution and patterns. Annu Rev Ecol Syst 28:341–358

    Article  Google Scholar 

  • Poulin R (1998) Evolutionary ecology of parasites: from individuals to communities. Chapman and Hall, London

    Google Scholar 

  • Poulin R, Morand S (2000) The diversity of parasites. Q Rev Biol 75:277–293

    CAS  PubMed  Google Scholar 

  • Purvis A, Rambaut A (1994) Comparative analysis by independent contrasts, CAIC version 2.0. Oxford University Press, Oxford

  • Rohde K (1998) Is there a fixed number of niches for endoparasites of fish? Int J Parasitol 28:1861–1865

    Google Scholar 

  • Rohde K, Heap M (1998) Latitudinal differences in species and community richness and in community structure of metazoan endo- and ectoparasites of marine teleost fish. Int J Parasitol 28:461–474

    Article  CAS  PubMed  Google Scholar 

  • Rosenzweig ML (1995) Species diversity in space and time. Cambridge University Press, Cambridge

  • Rosenzweig ML, Abramsky Z (1993) How are diversity and productivity related? In: Ricklefs RE, Schluter D (eds) Species diversity in ecological communities. University of Chicago Press, Chicago, Ill., pp 52–65

  • Ruvinsky I, Maxson LR (1996) Phylogenetic relationships among bufonoid frogs (Anura: Neobatrachia) inferred from mitochondrial DNA sequences. Mol Phyl Evol 5:533–547

    Article  CAS  Google Scholar 

  • Shurin JB, Allen EG (2001) Effects of competition, predation, and dispersal on species richness at local and regional scales. Am Nat 158:624–637

    Article  Google Scholar 

  • Shurin JB, Havel JE, Leibold MA, Pinel-Alloul B (2000) Local and regional zooplankton species richness: a scale-independent test for saturation. Ecology 81:3062–3073

    Google Scholar 

  • Sibley CG, Ahlquist JE (1990) Phylogeny and classification of birds. Yale University Press, New Haven, Conn.

  • Sousa WP (1994) Patterns and processes in communities of helminth parasites. Trends Ecol Evol 9:52–57

    Google Scholar 

  • Srivastava DS (1999) Using local-regional richness plots to test for species saturation: pitfalls and potentials. J Anim Ecol 68:1-16

    Article  Google Scholar 

  • Van der Meulen MA, Hudson AJ, Scheiner SM (2001) Three evolutionary hypotheses for the hump-shaped productivity-diversity curve. Evol Ecol Res 3:379–392

    Google Scholar 

  • Venterink HO, Wassen MJ, Belgers JDM, Verhoeven JTA (2001) Control of environmental variables on species density in fens and meadows: importance of direct effects and effects through community biomass. J Ecol 89:1033–1040

    Article  Google Scholar 

  • Waide RB, Willig MR, Steiner CF, Mittelbach G, Gough L, Dodson SI, Juday GP, Parmenter R (1999) The relationship between productivity and species richness. Annu Rev Ecol Syst 30:257–300

    Article  Google Scholar 

  • Walther BA, Cotgreave P, Price RD, Gregory RD, Clayton DH (1995) Sampling effort and parasite species richness. Parasitol Today 11:306-310

    Google Scholar 

  • Watve MG, Sukumar R (1995) Parasite abundance and diversity in mammals: correlates with host ecology. Proc Nat Acad Sci USA 92:8945–8949

    CAS  PubMed  Google Scholar 

  • Wiens JJ, Reeder TW (1997) Phylogeny of the spiny lizards ( Sceloporus) based on molecular and morphological evidence. Herpetol Monogr 11:1-101

    Google Scholar 

Download references

Acknowledgement

R. Poulin is supported by a James Cook Research Fellowship from the Royal Society of New Zealand. This study was supported by grant FONDECYT 1980442 to M. George-Nascimento.

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Correspondence to Robert Poulin.

Appendix 1

Appendix 1

Summary of the data set used in the analyses

Host species

No. hosts examined

Host mass (g)

Parasite richness

Log parasite biovolume/host

Genypterus maculatus

60

2,236

9

3.177

Genypterus chilensis

60

3,538

10

2.743

Genypterus blacodes

60

2,757

11

3.07

Hippoglossina macrops

25

810

7

1.017

Paralichthys adspersus

35

817

9

1.633

Paralichthys microps

35

568

9

1.55

Macruronus magellanicus

147

1,700

8

2.166

Merluccius australis

807

2,057

13

2.653

Merluccius gayi

578

890

13

2.322

Trachurus symmetricus

600

601

11

0.544

Dissostichus eleginoides

49

28,253

10

3.079

Stromateus stellatus

35

595

5

1.061

Eleginops maclovinus

75

1,136

12

1.496

Seriolella violacea

26

778

6

3.485

Scomber japonicus

77

1,372

8

1.009

Helicolenus lengerichi

56

1,136

11

1.584

Sebastes capensis

42

778

8

1.106

Brama australis

26

1,505

13

2.691

Thyrsites atun

17

1,161

8

1.27

Pinguipes chilensis

29

800

6

0.994

Prolatilus jugularis

35

400

9

1.29

Sicyases sanguineus

21

538

1

1.688

Scartichthys viridis

71

43

2

−0.854

Girella laevifrons

309

35

2

−1.523

Auchenionchus microcirrhis

22

46

2

−2.222

Graus nigra

73

33

2

−1.222

Cilus gilberti

57

5,447

15

2.623

Aplodactylus punctatus

46

814

4

2.086

Mugil cephalus

15

1,453

6

0.677

Gobiesox marmoratus

55

6

4

−1.523

Sindoscopus australis

43

2

3

−1.523

Calliclinus geniguttatus

30

5

5

−0.319

Myxodes cristatus

17

3

2

−0.538

Notothenia macrocephala

38

33

9

0.718

Epigonus crassicaudus

38

550

3

1.762

Auchenionchus variolosus

14

24

6

0.588

Myxodes viridis

15

4

6

0.602

Tripterygion chilensis

17

4

2

−0.538

Aphos porosus

22

204

9

0.9

Cheilodactylus variegatus

13

395

9

0.64

Bovichthys chilensis

14

513

6

2.056

Patagonotothen curnicola

58

10

10

1.015

Chamsocephalus gunnari

39

769

8

1.491

Bufo retiformis

49

12.5

6

1.583

Bufo cognatus

36

18.5

4

1.675

Bufo debilis

49

7

5

1.583

Bufo hemiophys

40

23

4

1.672

Spea multiplicata

31

26

4

0.795

Rana catesbiana

16

26

2

−0.027

Rana clamitans

62

200

5

1.119

Rana palustris

5

32

1

−1.398

Plethodon cinereus

60

25.5

4

0.358

Desmognathus brimleyorum

41

28

7

0.199

Desmognathus fuscus

52

9.5

3

−0.62

Eurycea bislineata

51

7

4

0.322

Rana pipiens

43

10

9

1.671

Nerodia cyclopion

48

208

12

4.126

Nerodia fasciata

30

183

10

2.448

Nerodia rhombifera

11

322

7

2.581

Agkistrodon piscivorus

10

199

10

3.167

Anolis aeneus

20

4

3

0.207

Anolis extremus

10

9

3

−0.523

Anolis gingivinus

78

3

9

0.947

Anolis griseus

10

13

3

0.258

Anolis luciae

34

5

3

1.176

Anolis marmoratus

25

4.5

3

−0.31

Anolis oculatus

20

6

8

0.863

Anolis richardi

20

13

4

0.452

Anolis trinitalis

17

3

1

−1.699

Anolis wattsi

20

2.5

4

−.222

Anolis carolinensis

30

7.5

2

0.322

Cnemidophorus dixoni

58

11.3

6

1.813

Cnemidophorus exanguis

37

13.5

3

1.525

Cnemidophorus gularis

118

10.5

6

1.234

Cnemidophorus neomexi

44

7.5

4

0.207

Cnemidophorus tesselatus

27

16.5

4

1.222

Sceloporus magister

17

534

6

0.79

Sceloporus meriami

39

79.5

3

−0.26

Sceloporus marriami

23

79.5

6

1.101

Sceloporus olivaceus

61

392.5

5

2.336

Sceloporus poinsettii

13

276

5

3.043

Sceloporus serrifer

25

438

4

1.916

Sceloporus undulatus

10

75.5

1

1.622

Urosouys ornatus

86

6.5

4

1.622

Alligator mississippiensis

50

750,000

11

2.435

Cnemidophorus burtistic

57

10.5

5

0.386

Barisia imbricata

14

9.5

4

1.498

Coerrhonotus ophiurus

54

16.5

3

1.37

Liolaemus lemniscatus

13

4

1

0.442

Liolaemus tenuis

7

5

1

1.15

Caretta caretta

54

10,700

5

2.506

Spermophylus townsendii

117

570

4

2.656

Eptesiicus fuscus

464

25

22

1.697

Lasionycteris noctivagans

6

15

5

1.917

Lasiurus borealis

90

13

5

1.979

Lasiurus cinereus

18

26

1

−0.143

Myotis keenii

30

6

8

1.742

Myotis lucifurgus

191

12

21

1.453

Myotis sodalis

17

11

9

2.447

Pipistrellus subflavus

71

5

8

−0.066

Hydrochaeris hydrochaeris

41

32,000

7

4.324

Clethrionomys glarealus

193

40

8

2.63

Oryzomys palustris

178

54

17

3.883

Rattus rattus

612

485

7

3.293

Canis latrans

177

23,000

20

2.029

Tadarida brasiliensis

45

13

10

1.384

Phocoena phocoena

80

60,000

7

3.589

Didelphis virginiana

46

4,020

12

3.396

Mustela vison

50

2,325

5

3.939

Ondatra zibethicus

50

1,370

3

2.291

Otaria flavescens

46

300,000

6

6.302

Aechmophorus occidentalis

20

1,262

16

4.105

Podiceps grisegena

33

1,124

20

4.609

Podiceps nigricollis

31

366

27

5.553

Podiceps auritus

7

393

14

3.583

Dendrocygna bicolor

30

688

15

2.938

Corus frugilegus

327

370

20

.886

Egretta caerulea

35

340

21

2.802

Ajaia ajaja

128

1,814

24

2.957

Edocinus albus

140

1,400

35

2.758

Accipiter striatus

8

323

5

0.88

Buteo lagopus

21

1,150

4

0.882

Buteo jamaicensis

11

995

5

1.306

Buteo platypterus

16

390

11

0.286

Falco sparverius

9

350

3

0.779

Puffinus gravis

15

4,080

8

2.601

Pandion haliaetus

5

1,600

14

3.625

Ixoreus naevius

46

110

21

1.808

Turdus migratorius

17

110

10

2.457

Phalacrocorax auritus

12

2,041

14

3.548

Phalacrocorax brasilianus

12

2,495

14

3.632

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Poulin, R., Mouillot, D. & George-Nascimento, M. The relationship between species richness and productivity in metazoan parasite communities. Oecologia 137, 277–285 (2003). https://doi.org/10.1007/s00442-003-1343-z

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