in avian community structure: in winter, species diversity is correlated with ..... failed to drop to at least -6øC during the 60+ yr of record (Thorp and Hinds 1977). ... lowship from the Northwest College and University Association for Science.
SEASONAL VARIATION STRUCTURE: MECHANISMS
IN AVIAN COMMUNITY DIFFERENCES IN REGULATING
DIVERSITY
J. T. ROTENBERRY, 1 R. E. FITZNER,2 AND W. H. RICKARD 2 •ShrubsteppeHabitat Investigation Team, Department of Biology, University of New Mexico, Albuquerque,New Mexico 87131 USA and 2PacificNorthwestLaboratory, Richland, Washington99352 USA
ABSTRACT.--Thirty avian censuseswere conducted over 2 yr along a wooded streamside in southcentralWashington. Avian speciesdiversity and richnessshow temporal periodicity (summer maxima and winter minima), but evennessdoesnot. Comparison with contemporaneouscensuses in adjoining shrubsteppeshowssubstantially greater diversity and richnessalong the streamside, while community evennessis greater in the shrubsteppe.We infer these conditionsto be a result of the arboreal physiognomyof the streamsideplant community. Comparing winter censusesto spring censuses,we observedstatisticallysignificantdifferences in avian community structure: in winter, speciesdiversity is correlated with evennessbut not richness,while in the breeding season,diversity varies as a function of richness,not evenness. Following a model proposedby Tramer (1969), we suggestthat community organization during the spring breeding seasonmay reflect elementsof resource-basedinterspecificcompetition, while winter assemblagesof birds are regulated by a harsh and variable climate. Received 3 April 1978, accepted21 February 1979.
THE relationship between species diversity and its components, richness and evenness, has been receiving increased attention (Peet 1974). Tramer (1969) has
proposed that changesin diversity may be mediated by changesin one or the other component and that these changes reflect alternative environmental conditions. He suggeststhat diversity changes with richness in relatively stable, benign environments and varies with evenness under unstable, rigorous conditions. The former occurs when most populations are near equilibrium, which is possiblebecause the physical environment and resource levels remain stable over time. Fluctuations in relative abundance are minimized, and variation depends on the addition or subtraction of species. Populations in variable, rigorous environments, on the other hand, are often held below equilibria by unfavorable conditions and may expand when conditions are alleviated. Such growth may be achieved by a variety of mechanisms (e.g. increased survival, immigration) and is likely to vary according to species.Tramer expects this variability in population numbers to influence consistently the distribution of relative abundances and, hence, community evenness. Tramer's hypothesis has been tested by Rotenberry (1978) and has been found to hold for a large set of bird census data ordered along a multidimensional gradient of climatic variability and harshness.
Tramer's hypothesisexplainslong-term yearly and/or large-scalegeographicvariation in avian community structure. Therefore, it seems reasonable to try to extend the same principles to account for observed seasonalvariations in local community organization. It is in this framework that we report the results of a series of bird censusestaken over a period of 2 yr in contrasting vegetation. STUDY AREA AND METHODS
Avifaunal censuseswere conducted in Snively Canyon, located on the Department of Energy's Arid Land Ecology (ALE) Reserve, Benton County, Washington, about 25 km northwest of Richland, Wash499 The Auk 96: 499-505. July 1979
500
ROTENBERRY, FITZNER, AND RICI,•RD
[Auk, Vol.96
:i:i::.:.:::.:..
Cot•mln
kmI
i
i
Fig. 1. Map ofsoutheastern Washington showing the location ofthe Snively Canyon survey area and
the extent ofshrubsteppe vegetation (stippled) throughout the region (modified from Daubenmire 1970).
ington (Fig. 1).The gulch isapproximately 2kmlong, varying from 10-75 mwide, and upto100 m deep. The small stream within the canyon ispermanent and isclosely bordered bytrees, Populus sp. and Salix sp., and deciduous shrubs, Prunus, Sambucus, Amelanchier, Rhus, Philadelphus, and others. Snively isisolated from similar arboreal vegetation byasurrounding matrix ofshrubsteppe vegetation
(Artemisia-Agropyron) (Daubenmire 1970) (Fig. 1).The nearest similar vegetation isfound along the Yakima River, -25 km distant.
Acensus route was run inthe morning (0700-0800 start) atintervals of2-6weeks from 19July 1974
to4August 1976. Itconsisted of12census stops about 200 mapart along the stream. Ateach stop all
birds identified orheard ina3-rain period were recorded. Because oftheshort distances between stops, carewastakentoavoid anydouble-counting ofindividuals.
Acompanion route was set upintypical shrubsteppe vegetation inApril 1976 inconjunction with another study. This route was consused asatypical cooperative breeding bird survey (Robbins and Van Velzen 1968): 3-rain stops, 0.8km(0.5 mi) apart, each sampled within a0.4-kin (0.25 mi) radius. Unlike the cooperative surveys, however, our route contained 25instead ofthe usual 50stops. Four such surveys were made inspring 1976 and three inspring 1977. Although these samples obviously counted more individuals than Snively surveys because oftheir substantially greater area ofcoverage, reduction ofthe datatorelative abundance allows a comparison between thetwotypes.
Species diversity was calculated according toSimpson (1949), then converted tothe equivalent number
ofequally common species byapplying areciprocal transformation. Thus,
Diversity = 1/• pi2,
where p,isthe relative abundance ofthe ith species inthe sample. This represents diversity asthe number ofequally abundant species occurring inasample that would produce the untransformed index previously calculated forthat sample. This has the advantages ofretaining "number ofspecies" asitsbasic unit, whileincluding theevenness component (Peet1974).
July 1979]
AvianCommunity Dynamics
501
The richnesscomponentis simply the numberof speciesin the sample. Evenness(the distributionof relative abundances amongthe speciessampled)was calculatedusinga ratio proposedby Hill (1973):
Evenness = Diversity/exp(• Pilog pi). The denominator is essentiallythe equivalent number of equally common speciesderived from the information theory measurefor speciesdiversity (Hill 1973). Equality of meanswas testedusingthe t'-test (Sokal and Rohlf 1969:374), which makesno assumptions concerningthe homogeneityof samplevariancesnor requiresequal samplesizes. Partial coefficientsof determination(ggpart)were usedto assessthe separatecontributionsof richness and evennessto "explaining" variation in diversity (Steel and Torrie 1960). Becausethe calculationof diversity is mathematically not independent of values of richnessand evenness,correlation analysis of variation in diversity with respectto those two variables is inappropriate. RESULTS
The results of 21 of the 30 Snively Canyon surveys are summarized in Table 1 and include only those speciesthat averaged at least one individual per count on either 11 breeding-season(May-August) or 10 wintering-season(November-March) counts. These speciescomprise 91.4% of all individuals seen during the breeding seasonand 82.7% of all seen during the winter. Breeding-seasonsurveysaveraged 148 individuals of 19.5 speciesper count, while winter surveys averaged 59 individuals of 11.3 species. Altogether, 81 species were recorded from all 30 counts combined. Similarly, the resultsof 7 breeding seasonshrubsteppetransectsare given in Table 1. An averageof 10.3 speciesand 385 individualswas seen,with 29 species recorded altogether. Community statisticsfor the Snively Canyon surveys (separated by season)and the shrubsteppetransectsare summarizedand comparedin Table 2. Substantially more individuals were seen per shrubsteppetransect compared to Snively, most likely a function of the substantially larger area covered. Nevertheless, the average number of speciesseenwas only - 10, significantlylessthan that observedon spring season canyon surveys. Likewise, diversity was significantly lower in the shrubsteppe than in the canyon, although evennesswas significantly higher. Within the canyon, the winter bird assemblageconsistsof significantly fewer individuals and speciesat a lower diversity than does the breeding-seasonassemblage,although evennessdoes not appear to differ between the two samples. Figure 2 summarizesthe descriptivestatisticsof the Snively Canyon bird community as sampled through time. The periodicity of both richnessand diversity is quite apparent (Fig. 2A); both achieve maximum values during the breeding season and minima during mid-winter. Community evennessshowsa substantially different pattern (Fig. 2B); periodicity is undetectable, with maxima being attained between mid-November and early March 1975-76. Minimum values, however, occurred in the same time period the previous winter. DISCUSSION
Arboreal/shrubsteppe comparisons.--Althoughit is often difficult to make new usesof data collectedfor other purposes, comparisonof the Snively Canyon censuses with thoseconductedin the nearby shrubsteppedoesallow us to make severalpoints
concerningthe mechanismswe think are important in structuringthe Snively bird community. For example, Table 2 clearly shows the greater richnessand diversity of Snively Canyon breeding avifauna compared to that of the adjacent shrubsteppe.
502
ROTENBERRY, FITZNER,AND R•ICKARD
[Auk, Vol. 96
TABLE1. Dominantspecies of birdsrecordedon SnivelyCanyonand shrubsteppe surveys.Valuesare averagenumberof individualsseenfor 11 breeding-season (May-August)and 10 wintering-season (November-March)countsin the canyon,and 7 breeding-season countsin the shrubsteppe. Actual number of countson which each specieswas observedis in parentheses.
SnivelyCanyon,breeding
SnivelyCanyon,wintering
Kestrel
California Quail
(Falcosparverius) SageGrouse (Centrocercus urophasianus)
1.0
(7)
1.4
(2)
California Quail
(Lophortyxcalifornicus)
Chukar
(Alectorischukar) MourningDove (Zenaidamacroura) EasternKingbird (Tyrannustyrannus)
(Picapica)
Rock Wren
(Salpinctes obsoletus) Starling (Sturnusvulgaris)
1.8
(6)
20.7
(9)
28.5
(11)
1.9
(5)
8.9
(11)
5.2
(10)
1.0
(7)
5.6
(5)
( Wilsonia pusilla)
1.1
(6)
3.7
(4)
(Molothrus ater)
I. 1
(3)
(Icterus galbula)
7.6
(10)
Western Tanager (Piranga ludoviciana) LazuliBunting (Passerina amoena) Vesper Sparrow (Pooecetes gramineus) White-crowned Sparrow (Zonotrichia leucophrys) Song Sparrow (Melospizamelodia) 38 other species
(5)
1.1
(4)
2.2
(8)
2.6
(6)
1.2
(6)
(Dendroicacoronata) WesternMeadowlark
4.7
(2)
(Sturnellaneglecta)
3.7
(5)
26.5
(9)
1.8
(5)
1.6
(7)
(Eremophilaalpestris)
Black-billed Magpie
(Pica pica) AmericanRobin (Turdusmigratorius) Ruby-crownedKinglet (Reguluscalendula)
Dark-eyed Junco
(Juncohyemalis) White-crowned Sparrow (Zonotrichialeucophrys) (Melospizamelodia) 20 other species
(Sturnella neglecta) 19.4 (11) Brewer's Blackbird (Euphagus cyanocephalus) 2.8 (6) Brown-headed Cowbird Northern Oriole
1.7
Song Sparrow
Wilson's Warbler
Western Meadowlark
(1)
Yellow-rumped Warbler
Yellow-breated Chat
(Icteria virens)
1.5
Horned Lark
Barn Swallow
(Hirundorustica) Black-billedMagpie
(Lophortyxcalifornicus) Ring-necked Pheasant (Phasianuscolchicus)
1.5 (5) 5.5 (10) 7.4 (7) 1.0
(1)
1.4
(7)
10.2
Shrubsteppe, breeding
GreyPartridge (Perdix perdix) Mourning Dove (Zenaida macroura) HornedLark
(Eremophila alpestris)
Western Meadowlark
1.0 (2) 2.1 (7) 150.1 (7)
(Sturnella neglecta) 144.1 (7) Vester Sparrow (Pooecetes gramineus) 9.6 (7) Sage Sparrow (Amphispiza belli) 65.5 (7) White-crowned Sparrow (Zonotrichia leucophrys) 5.6 (2) 22other species 7.0
12.1
This is mostlikely a reflectionof the well establishedrelationshipbetweenvegetation structureand bird speciesdiversity.Studiesencompassing a wide rangeof habitat
types(e.g.MacArthur1964,Karr and Roth 1971)havedemonstrated anddiscussed this correlation,and Willson(1974)hassuggested that it reflectsthe additionof new species throughthe accumulation of new guildsin a stepwise fashionasvegetation complexity increases.
Althoughit seemsintuitivelylikely that the woodedstreamside permitsthe existenceof a greaternumberof structurally-oriented guildsthan the physiognomically simplershrubsteppe, that the mechanism suggested by Willson(1974)is apparently operatinghereis substantiated by the observation that whilediversityand richness are greaterin arborealvegetation,evennessis not (Table 2), and that increased diversityis associated with increasedrichness(i.e. the additionof new species),not increased
evenness.
July 1979]
AvianCommunity Dynamics
A
--
Richness
/xe ---Diversity
25
•
503
•0
o
=
10
5
B •o
0,90
k-
0.50
d
d A
S 1974
Fig. •.
0
ND
F M
A
MU 1975
d
A S
0
N
D
F M A
M d
d
A
1976
5ea•onal variation in bird communtt• attr•bute• of •nive}• Can•on; A•dchne•
and diversity;
B•venness.
Seasonaldynamics.--Thelack of periodicityin the evenness data (Fig. 2B), particularlywhen considered in conjunctionwith the distinctseasonality evidencedby richnessand diversity, leads to sometentative conclusions regardingfactorsthat may regulate community diversity. We observedthat while the difference in evennessbetween both setsof winter counts(November-March 1974-75 and 1975-76)
is highly significant(P < 0.001), it is not reflectedin diversity(P > 0.05). Neither is there a significantdifferencein richnessbetweenthe two years. Examination of the partial coefficientsof determinationshowsthat during the winter, diversityclearlyvariesas a functionof evenness (g2par!= .91) and is quite independentof changesin richness(R2p•,.t= .17). A distinctlydifferent pattern, however, is evidencedduring the breedingseason:diversity becomesmuch more highlyassociated with richness(g2part= .87) and is lessso with evenness (g2part= ß72). This stronglysuggests that we are observingdifferent methodsof "regulation" of communitystructureat the samesite, which may vary accordingto season. Comparing the two seasons,resourcesduring the breedingseasonare likely to be morestablethan theyare in winter, the vegetationstructuremorecomplex,and the climate more benign. Winter weather in the arid interior regionsof the northwest
504
ROTENBERRY, FITZ•ER, ANDRICKARD
[Auk, Vol. 96
TABLE 2. Comparisonof mean avian community attributes of Snively Canyon breedingand wintering seasonsurveysand adjacent shrubsteppebreedingseasonsurveys.Asterisksdenotethe probability that two adjacentmeansin a columnare different(* = P • 0.95; ** = P • 0.99; *** = P • 0.999). Number of indi-
Area
Snively Canyon
Shrubsteppe
Season
viduals
Richness
Evenness
Diversity
59
! 1.3
0.70
4.4
Breeding (n = 11)
148
19.5
0.67
6.8
Breeding (n = 7)
385
10.3
0.82
2.9
Winter (n = 10)
can vary considerablyand is often rigorous. For example, long-term weather data collectedwithin 15 km of SnivelyCanyonshowthat winter minimum temperatures are more variable than summer maxima (a range of 27øCversus8øC)and have never
failed to drop to at least-6øC duringthe 60+ yr of record(Thorp and Hinds 1977). Under summerconditionsit is not unreasonable to expectthat populationsare nearer their localequilibriumvalues(determinedby resourcestates,vegetationcomplexity, etc.) than in winter and that the communityorganizationmight then be more likely to reflect elements of resource-basedinterspecific competition. Indeed, such com-
petition and subsequenthabitat partitioningis generallyassumedto be the driving force behind the relationshipbetween bird speciesdiversity and vegetationcomplexity(MacArthur 1964,Karr and Roth 1971).Again, we suggestthat thisdiversity/ complexityrelationshipaccountsfor the greater variety of breedingbirds in Snively Canyon compared to the shrubsteppe. Kricher (1975) found in the simple systemhe observedthat winter diversity [as well as summer diversity (Kricher 1972)] varied with richnessrather than evenness. He concludedfrom this that severeweather, rather than exerting direct effectson bird species,worked indirectlyby reducingfood supplies.Conversely,the diversity patterns we observedcertainly suggestthat bird populationshave the potential for regulation of their numbers outside those determined by their resourcebase. The difference between Kricher's observations and ours is likely related to differencesin the scaleof sampling. His data were gathered in two separatesuccessional stagesthat differed in vegetation structure as well as microclimate. Additionally, it seemsprobable that winter weather variation between his plots (separated by -1 km) was much lessextreme than the difference between summer and winter in our samples.
In any event, the patterns we have observed are statistically valid and logically consistentwith Tramer's hypothesis.They point out the likelihood, often ignored, that examination of a community through its seasonalchangesmight easily suggest variation in the causal mechanisms that structure that community. ACKNOWLEDGMENTS
This work was done by Pacific Northwest Laboratories for the U.S. Department of Energy under Contract AT(45-1)-1830. Rotenberry was supported by USDOE Contract E(45-1)-2042 while on a fellowship from the Northwest Collegeand University Associationfor Science. LITERATURE
DAUBENMIRE, R. Bull. 62.
CITED
1970. Steppe vegetation of Washington. Washington Agr. Exp. Station Tech.
July1979]
AvianCommunity Dynamics
505
HILL, M. O. 1973. Diversity and evenness:a unifying notation and its consequences.Ecology 54: 427432.
KARR, J. R., & R. R. ROTH. 1971. Vegetation structure and arian diversity in several New World areas. Amer.
Natur.
105: 423-435.
KRICHER,J. C. 1972. Bird speciesdiversity: the effect of speciesrichnessand equitability on the diversity index. Ecology 53: 278-282. 1975. Diversity in two wintering bird communities: possibleweather effects. Auk 92: 766-777. MACARTHUR, R. H. 1964. Environmental factors affecting bird speciesdiversity. Amer. Natur. 98: 387-397.
PEET, R. K. 1974. The measurementof speciesdiversity. Ann. Rev. Ecol. Syst. 5: 285-307. ROBBINS,C. S., & W. T. VAN VELZEN. 1967. The breedingbird survey, 1966. U.S. Dept. Interior, Fish. Wildl. Serv., Spec. Sci. Rep., Wildl. No. 102. ROTENBERRY,J. T. 1978. Components of avian diversity along a multifactorial climatic gradient. Ecology 59: 693-699. SIMPSON, E. H. 1949. Measurement of diversity. Nature 163: 688. SOKAL,R. R., & F. J. ROHLF. 1969. Biometry. San Francisco, W. H. Freeman and Co. STEEL, R. G. D., & J. H. TORRIE. 1960. Principlesand proceduresof statistics.New York, McGrawHill Book Co., Inc. THORP, J. M., & W. T. HINDS. 1977. Microclimates of the Arid Lands Ecology Reserve, 1968-1975. Richland, Washington, Battelle, Pacific Northwest Laboratories. BNWL-SA-6231. TRAMER, E. J. 1969. Bird speciesdiversity: componentsof Shannon'sformula. Ecology 50: 927-929. WILLSON, n. F. 1974. Avian community organization and habitat structure. Ecology 55: 1017-1029.
