Cited by 730Ecology and Vegetation Dynamics StudiesInsect and Arachnid Ecology and BehaviorForest Ecology and Biodiversity Studies

The DOI matches its Crossref record; 142 of the 146 references it cites were found in a registry or an index; none of the 145 sources its claims cite is checked for support yet.

Climate-driven declines in arthropod abundance restructure a rainforest food web

Open access
Lister, Bradford C., Garcia, Andres·2018·Proceedings of the National Academy of Sciences

Abstract

Significance: Arthropods, invertebrates including insects that have external skeletons, are declining at an alarming rate. While the tropics harbor the majority of arthropod species, little is known about trends in their abundance. We compared arthropod biomass in Puerto Rico’s Luquillo rainforest with data taken during the 1970s and found that biomass had fallen 10 to 60 times. Our analyses revealed synchronous declines in the lizards, frogs, and birds that eat arthropods. Over the past 30 years, forest temperatures have risen 2.0 °C, and our study indicates that climate warming is the driving force behind the collapse of the forest’s food web. If supported by further research, the impact of climate change on tropical ecosystems may be much greater than currently anticipated.

Overview

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Written from the paper’s full text.

TL;DR

Long-term data from Puerto Rico’s Luquillo rainforest show arthropod biomass fell sharply between the 1970s and 2010s, with synchronous declines in insectivorous lizards, frogs, and birds. The authors argue climate warming, especially rising maximum temperatures, is the likely driver of a bottom-up food-web collapse.

Key findings

  • Arthropod biomass declined across sampling methods: sweep-net biomass fell 4× in July and 8× in January; ground sticky-trap catch fell 36× from 473 to 13 mg per trap per day in July and about 60× from 470 to 8 mg per trap per day in January; canopy trap catch fell from 37 to 5 mg per trap per day in July.
  • All 10 major arthropod taxa in sweep samples declined proportionately (Kolmogorov–Smirnov z = 0.671, P = 0.759), and all 10 most-abundant canopy taxa showed negative trends from 1990–2010 (binomial probability = 0.00097).
  • Forest maximum temperature at El Verde rose 2.0 °C from 1978–2015 at 0.050 °C/y; at Bisley Tower the rate was 0.055 °C/y. At Bisley, the proportion of daily maximum temperatures ≥29.0 °C averaged 0.03 in 1993–1994 and 0.44 in 2014–2015, a 14-fold increase while average temperatures rose 8–10%.
  • Insectivores declined: anole density fell about 2.2×, from 12,490 to 5,640 anoles per hectare, and anole biomass dropped 32%, from 401 g to 277 g; A. evermanni declined 10× and A. stratulus disappeared from sampled habitats. Insectivorous bird captures fell 53%, from 137 birds in 1990 to 64 in 2005, and the Puerto Rican tody declined 90%.
  • In Mexico’s Chamela-Cuixmala dry forest, ground-trap arthropod biomass fell 8× in 2014 compared with July 1987–1988 averages.

Methods

  • The study compared arthropod samples from the same Luquillo study area in July 1976 and January 1977 with samples from July 2011–2012 and January 2012–2013, using sticky traps and sweep nets; it also analyzed Luquillo LTER datasets on canopy arthropods, walking sticks, E. coqui, and birds.
  • Climate data came from El Verde Field Station (1978–2015) and Bisley Tower (1993–2014), using daily maximum temperatures; analyses included quasi-Poisson regressions, hierarchical partitioning, cross-correlation with the Southern Oscillation Index, and Vinod causality.
  • Additional comparisons used the same sticky-trap methods in Chamela-Cuixmala Biosphere Reserve, Mexico, in 2014 versus 1986–1987 samples.

Limitations

  • Stated: no climate data were available at Bisley Tower until 1993, so E. coqui abundance could not be regressed against temperature there; the meteorological stations recorded only one maximum and minimum per 24 h, so the duration of temperatures above 29 °C could not be calculated; the extent to which altitudinal range shifts influenced the observed declines is unknown.
  • Stated: the causal inference is observational, and the authors note that regression and correlation analyses leave causality open to question, using Vinod causality as a statistical aid rather than experimental proof.
  • Evident: the study relies on historical datasets collected by different researchers over decades, and although methods were matched where possible, the design cannot fully exclude unmeasured factors such as hurricanes, droughts, ENSO variation, or other environmental changes.

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Registry

Crossref · 10.1073/pnas.1722477115

Cites

142 of 142 references verified0 citation errors · 0 not checkable

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Figures

Fig. 1. Air temperature trends within the Luquillo forest. MnMaxT vs. year for the (A) El Verde (1978–2015) and (B) Bisley Tower (1994–2012) meteorological stations. The stations are ∼8.2 km apart at elevations of 350 and 352 m, respectively. The least-squares regression lines have been drawn through the data points. The difference between the slopes of the two regression lines is not significant (t = 0.281, P = 0.78).
Fig. 1. Air temperature trends within the Luquillo forest. MnMaxT vs. year for the (A) El Verde (1978–2015) and (B) Bisley Tower (1994–2012) meteorological stations. The stations are ∼8.2 km apart at elevations of 350 and 352 m, respectively. The least-squares regression lines have been drawn through the data points. The difference between the slopes of the two regression lines is not significant (t = 0.281, P = 0.78).CC BY-NC-ND · PubMed Central
Fig. 2. Mean dry-weight arthropod biomass per 100 sweeps taken in the same sample area in the Luquillo rainforest during July 1976, January 1977, July 2011, and January 2013. One SE around the mean biomass is shown for each bar. Total sweeps taken in each period was 800, except for July 1976, when 700 sweeps were taken. Data for 1976 and 1977 are from Lister (22).
Fig. 2. Mean dry-weight arthropod biomass per 100 sweeps taken in the same sample area in the Luquillo rainforest during July 1976, January 1977, July 2011, and January 2013. One SE around the mean biomass is shown for each bar. Total sweeps taken in each period was 800, except for July 1976, when 700 sweeps were taken. Data for 1976 and 1977 are from Lister (22).CC BY-NC-ND · PubMed Central
Fig. 3. Comparison of total dry-weight biomass for the major arthropod taxa captured in sweep samples taken during the summer (A, C, and E) and winter (B, D, and F) seasons 1976–1977 and 2011–2013, within the same Luquillo forest study area. Arn, Areneida; Col, Coleoptera; Dip, Diptera; For, Formicidae; Hem, Hemiptera; Hom, Homoptera; Hym, other Hymenoptera; La, Lepidoptera adults; LI, Lepidoptera larvae; Ort, Orthoptera.
Fig. 3. Comparison of total dry-weight biomass for the major arthropod taxa captured in sweep samples taken during the summer (A, C, and E) and winter (B, D, and F) seasons 1976–1977 and 2011–2013, within the same Luquillo forest study area. Arn, Areneida; Col, Coleoptera; Dip, Diptera; For, Formicidae; Hem, Hemiptera; Hom, Homoptera; Hym, other Hymenoptera; La, Lepidoptera adults; LI, Lepidoptera larvae; Ort, Orthoptera.CC BY-NC-ND · PubMed Central
Fig. 4. Comparison of the average dry-weight biomass of arthropods caught per 12-h day in 10 ground (A) and canopy (B) traps within the same sampling area in the Luquillo rainforest. Numbers above the bars give the mean daily catch rate in dry weight of arthropods per day for the respective dates. Data for 1976 and 1977 are from Lister (22).
Fig. 4. Comparison of the average dry-weight biomass of arthropods caught per 12-h day in 10 ground (A) and canopy (B) traps within the same sampling area in the Luquillo rainforest. Numbers above the bars give the mean daily catch rate in dry weight of arthropods per day for the respective dates. Data for 1976 and 1977 are from Lister (22).CC BY-NC-ND · PubMed Central
Fig. 5. Trends in the abundance of canopy arthropods and walking sticks in the Luquillo forest El Verde study area. (A) Linear regression of the total number of canopy arthropods captured per foliage weight sampled at El Verde against the period when the samples were taken. (B) Cubic regression for the total number of canopy arthropods captured per foliage weight sampled against the MnMaxT during the period when the samples were taken. (C) Quasi-Poisson regression of total number of walking sticks vs. the period when the population was sampled. (D) Quasi-Poisson regression of total number of walking sticks vs. the MnMaxT during the period when the population was sampled. The 95% confidence intervals are shown around the best-fit regression lines. For the Poisson regressions, Pr(χ) is the result of a likelihood-ratio χ2 test of whether the independent variable improves the Poisson model beyond an intercept-only model. P < 0.05 indicates a statistically significant regression.
Fig. 5. Trends in the abundance of canopy arthropods and walking sticks in the Luquillo forest El Verde study area. (A) Linear regression of the total number of canopy arthropods captured per foliage weight sampled at El Verde against the period when the samples were taken. (B) Cubic regression for the total number of canopy arthropods captured per foliage weight sampled against the MnMaxT during the period when the samples were taken. (C) Quasi-Poisson regression of total number of walking sticks vs. the period when the population was sampled. (D) Quasi-Poisson regression of total number of walking sticks vs. the MnMaxT during the period when the population was sampled. The 95% confidence intervals are shown around the best-fit regression lines. For the Poisson regressions, Pr(χ) is the result of a likelihood-ratio χ2 test of whether the independent variable improves the Poisson model beyond an intercept-only model. P < 0.05 indicates a statistically significant regression.CC BY-NC-ND · PubMed Central
Fig. 6. Comparison of anoles censuses conducted in the same Luquillo rainforest study area during July 1976 and January 1977, with censuses conducted during July 2011 and January 2012. The total number of anoles in each census, estimated by the Schnabel multiple capture–recapture method (27), is given above each histobar. Brown represents male and female A. gundlachi. Green represents A. evermanni. Gray represents A. stratulus. SI Appendix, Table S1 gives the 95% confidence intervals around estimated abundances for A. gundlachi and A. evermanni.
Fig. 6. Comparison of anoles censuses conducted in the same Luquillo rainforest study area during July 1976 and January 1977, with censuses conducted during July 2011 and January 2012. The total number of anoles in each census, estimated by the Schnabel multiple capture–recapture method (27), is given above each histobar. Brown represents male and female A. gundlachi. Green represents A. evermanni. Gray represents A. stratulus. SI Appendix, Table S1 gives the 95% confidence intervals around estimated abundances for A. gundlachi and A. evermanni.CC BY-NC-ND · PubMed Central
Fig. 7. Population trends for E. coqui and birds near the El Verde Field station. (A) Quasi-Poisson regression of estimated total number of E. coqui individuals against time from censuses conducted by Stewart (28) in the Activity Transect. (B) Quasi-Poisson regression of the estimated number of E. coqui individuals against MnMaxT during the time periods when Stewart’s censuses were conducted. (C) Quasi-Poisson regression for the total number of birds captured during equal length, 4-d sessions of mist netting (31) near the El Verde Field Station against the period when the mist netting was conducted. (D) Quasi-Poisson regression of the total number of birds captured during Waide’s (31) 4-d sessions vs. MnMaxT during the year of mist netting. The 95% confidence intervals are shown around the best-fit regression lines. Pr(χ) is the result of a likelihood-ratio χ2 test of whether the independent variable improves the model beyond an intercept-only model. P < 0.05 indicates a statistically significant regression.
Fig. 7. Population trends for E. coqui and birds near the El Verde Field station. (A) Quasi-Poisson regression of estimated total number of E. coqui individuals against time from censuses conducted by Stewart (28) in the Activity Transect. (B) Quasi-Poisson regression of the estimated number of E. coqui individuals against MnMaxT during the time periods when Stewart’s censuses were conducted. (C) Quasi-Poisson regression for the total number of birds captured during equal length, 4-d sessions of mist netting (31) near the El Verde Field Station against the period when the mist netting was conducted. (D) Quasi-Poisson regression of the total number of birds captured during Waide’s (31) 4-d sessions vs. MnMaxT during the year of mist netting. The 95% confidence intervals are shown around the best-fit regression lines. Pr(χ) is the result of a likelihood-ratio χ2 test of whether the independent variable improves the model beyond an intercept-only model. P < 0.05 indicates a statistically significant regression.CC BY-NC-ND · PubMed Central

Verification

Claims the paper makes

95 Not checked yet · 47 Own result · 18 Own interpretation · 7 Own method · 3 No basis given

Verify all 145 references — free account

Show all 69 claims

  • It may state two separate claims as one. 57
  • Probably not a substantial claim. 64
101 of 101
  • The paper relies on this without support.

    The historical data from the 1970s and other earlier censuses are comparable to the authors’ later samples despite the time gap and any differences in observers or methods.

    “We compared arthropod biomass in Puerto Rico’s Luquillo rainforest with data taken during the 1970s and found that biomass had fallen 10 to 60 times.”
    “Data for 1976 and 1977 are from Lister (22).”
  • The paper relies on this without support.

    The meteorological stations at El Verde and Bisley adequately represent the temperature exposure of the arthropod and insectivore populations studied.

    “Fig. 1 compares trends in mean maximum yearly temperature (MnMaxT) for the El Verde Field Station and Bisley Tower meteorological stations, both located at an altitude of 350 m.”
    “The stations are ∼8.2 km apart at elevations of 350 and 352 m, respectively.”
  • The paper relies on this without support.

    The statistical associations between temperature and abundance are not confounded by unmeasured variables that could produce the observed relationships.

    “Regression and correlation analyses inevitably leave the issue of causality open to question (33, 34). In lieu of intractable experiments spanning large spatial and temporal scales, Vinod causality offers a statistical method that can help identify causal variables and reveal the direction of causal paths (36).”
  • The paper relies on this without support.

    The eruption of Mount Pinatubo lowered global temperature by as much as 0.6 °C over the next 2 y.

    “the eruption of Mount Pinatubo, which lowered global temperature by as much as 0.6 °C over the next 2 y, occurred during the walking stick, Sonadura West, and Sonadura Old censuses.”
  • The paper relies on this without support.

    The climate data from the El Verde and Bisley meteorological stations are representative of the study area's climate.

    “The El Verde station lies 5 km southwest of our study area (18.3211° N, 65.8200° W), at an elevation of 350 m. The upper Bisley Tower is located 3.2 km southeast of our study area (18.3164 N, 65.7453 W) at 352 m in elevation.”
  • The paper relies on this without support.

    The Luquillo LTER data sets used are accurate and comparable over time.

    “Data sets from the Luquillo long-term ecological research (LTER) online Data Center were downloaded and analyzed for trends in population abundances over time.”
  • The paper relies on this without support.

    The 11 climate-related indices constructed from LTER temperature and rainfall data capture the relevant climate variation for the taxa studied.

    “we constructed 11 climate-related indices from the Luquillo LTER temperature and rainfall data for use in HP and regression analyses.”
  • The paper relies on this without support.

    Changes in temperature often lag phase shifts in the SOI by up to 9 months.

    “Changes in temperature often lag phase shifts in the SOI by up to 9 mo, and this effect may be partly responsible.”
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  • Not confirmedz = 0.671reported p = .759 · recomputed p = .502

    “z = 0.671, p = .759”

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Citations

Cites

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Research works printed but not linked: 5

  1. , eds ML Parry, OF Canziani, JP Palutikof, PJ van der Linden, CE Hanson (Cambridge Univ Press, Cambridge, UK Contribution of Working Group II to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change, 2007).
  2. R Joglar P Burrowes Declining amphibian populations in Puerto Rico. Contributions to West Indian Herpetology: A Tribute to Albert Schwartz Contributions to Herpetology eds Powell R Henderson RW (The Society for the Study of Amphibians and Reptiles Ithaca NY) Vol 12 pp 371–380. (1996).
  3. JA Pounds, Disappearing gold. BBC Wildlife 8, 812–817 (1990).
  4. JA Pounds, Amphibian watch: New clues in the case of the disappearing amphibians. Wildlife Conservation 94, 16–18 (1991).
  5. P Burrowes, A Longo, R Joglar, Geographic distribution of Batrachochytrium dendrobatidis in Puerto Rico. Herpetol Rev 39, 321–324 (2008).

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Metadata

Authors
Lister, B. C., & Garcia, A.
Affiliations
  • Rensselaer Polytechnic Institute (US)
  • Estación de Biología Chamela, Instituto de Biología, Universidad Nacional Autónoma de México, 47152 Chamela, Jalisco, Mexico
Corresponding author
Lister, Bradford C.
Venue
Proceedings of the National Academy of Sciences
Published
2018-10-15
Volume
115
Issue
44
Pages
E10397-E10406
ISSN
  • 0027-8424 (ISSN-L)
  • 1091-6490
OpenAlex
W2896548525
Cited by
730
References
146
Citations by year
2026: 37 · 2025: 60 · 2024: 67 · 2023: 99 · 2022: 81 · 2021: 122 · 2020: 122 · 2019: 137 · 2018: 4
FWCI
75.51
Type
journal article
Language
en
Open access
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by-nc-nd)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
Funders
NSF (1038013)
Topics
  • Physical Sciences › Environmental Science › Nature and Landscape Conservation › Ecology and Vegetation Dynamics Studies
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Insect and Arachnid Ecology and Behavior
  • Life Sciences › Agricultural and Biological Sciences › Insect Science › Forest Ecology and Biodiversity Studies
Keywords
global warming, insectivores, ENSO, Luquillo Experimental Forest, long-term ecological monitoring, canopy arthropods, walking stick, lizards, frogs, birds, Puerto Rico
MeSH terms
Animals, Arthropods, Birds, Puerto Rico, Trees, Tropical Climate, Ecosystem, Biomass, Food Chain, Biodiversity, El Nino-Southern Oscillation, Forests, Rainforest

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