Advertisement

Oecologia

, Volume 187, Issue 2, pp 483–494 | Cite as

Temperature effects on a marine herbivore depend strongly on diet across multiple generations

  • Janine Ledet
  • Maria Byrne
  • Alistair G. B. Poore
SPECIAL TOPIC: FROM PLANTS TO HERBIVORES

Abstract

Increasing sea surface temperatures are predicted to alter marine plant–herbivore interactions and, thus, the structure and function of algal and seagrass communities. Given the fundamental role of host plant quality in determining herbivore fitness, predicting the effects of increased temperatures requires an understanding of how temperature may interact with diet quality. We used an herbivorous marine amphipod, Sunamphitoe parmerong, to test how temperature and diet interact to alter herbivore growth, feeding rates, survival, and fecundity in short- and long-term assays. In short-term thermal stress assays, S. parmerong was tolerant to the range of temperatures that it currently experiences in nature (20–26 °C), with mortality at temperatures > 27 °C. In longer term experiments, two generations of S. parmerong were reared in nine combinations of temperature (ambient, + 2, + 4 °C) and diet (two high- and one low-quality algal species) treatments. Temperature and diet interacted to determine total numbers of amphipods in the F1 generation and the potential F2 population size (sum of brooded eggs and newly hatched juveniles). The size and development rate of F1 individuals were affected by diet, but not temperature. Consumption rates per capita were highest at intermediate temperatures but could not explain the observed differences in survival. Our results show that predicting the effects of increasing temperature on marine herbivores will be complicated by variation in host plant quality, and that climate-driven changes to plant availability will affect herbivore performance, and thus the strength of plant–herbivore interactions.

Keywords

Herbivory Macroalgae Amphipods Survival Climate change 

Introduction

Changes to the strength of species interactions in a warming world are likely to profoundly reshape biological communities (Kordas et al. 2011; Ockendon et al. 2014). Warming is resulting in novel species interactions due to the global redistribution of many taxa (Pecl et al. 2017) and altering the interactions between consumers and their prey, between pathogens and their hosts, and among competitors (Davis et al. 1998; Eisenlord et al. 2016). Warming-induced changes to the strength of plant–herbivore interactions, in particular, have the potential to dramatically alter landscapes in terrestrial (Tylianakis et al. 2008) and marine ecosystems (Vergés et al. 2014).

Predicting the outcomes of warming on plant–herbivore interactions, however, is complicated by a potentially diverse set of direct and indirect interactions (Fig. 1, Lemoine et al. 2013; Cross et al. 2015). Consumption experiments with single food plants do not capture these possible interactions as the effects of temperature and food quality are not always independent (Stamp and Bowers 1990). In addition to altering consumption rates, warming can alter feeding preferences among available plants (Lemoine et al. 2013; Schram et al. 2015) and force individual herbivores to make habitat choices that minimize exposure to thermal stresses (Burnaford 2004). Interactions between diet quality and temperature can arise, with differences in herbivore performance between the diets that support the best and worst performance often larger at higher temperatures (Lee and Roh 2010), and the effect of plant secondary metabolites on herbivore performance is often temperature-dependent (Stamp and Yang 1996). Herbivore growth and fitness is also dependent on the availability of preferred food sources, which can be influenced by temperature (Cleland et al. 2007; Lemoine and Burkepile 2012; Cross et al. 2015). Altered physiology at higher temperatures, such as decreased nitrogen digestibility and increased turn-over of proteins in herbivore tissues, can result in nitrogen limitation (Lemoine and Shantz 2016). These effects can cascade through the food web and generate nonlinear outcomes for ecosystems linked to elevated temperature. The complexity of responses of herbivores to warming and possible indirect effects through alterations to food quantity (Fig. 1) and quality impedes our ability to predict long-term effects of either climate change (Helmuth et al. 2005; Kingsolver and Huey 2008) or seasonal variation (Burrows et al. 2011; Sotka and Reynolds 2011).
Fig. 1

Direct (solid lines) and indirect (dashed lines) links between temperature and the trophic interactions among plants, herbivores, and their predators. We examined the direct effect of temperature on (a) herbivores (feeding, survival and fecundity), (b) consumption of plants (evaluating herbivore population size and per capita feeding rates), and (c) effects of variation in plant quality to herbivores (black lines). Other interactions that could affect the levels of top–down control of plants by herbivores under changing temperatures include: (d) direct effects of temperature on plant abundance and tissue qualities, (e) direct effects of temperature on predator abundance and metabolism, and (f) predator control of herbivore populations (a function of predator abundance and per capita feeding rates). These lead to a complex set of possible indirect interactions, including: (h) temperature indirectly affecting plant abundance due to changes in herbivore populations and or feeding rates (changes to direct effects a and b), (i) temperature indirectly affecting herbivore populations due to changes in plant abundance or quality (changes to direct effects d and c) or the likelihood of trophic cascades (changes to direct effects e, g, and b) and (j) temperature indirectly affecting predators due to any changes in herbivore abundance (changes to direct effects d, c, and g). See Fig. S3. for scenarios that differ in their temperature effects on survival and consumption

Given the need to consider how temperature may interact with diet, this study investigated the short- and long-term effects of temperature and varying algal diets on a marine plant–herbivore interaction. The top–down control of macroalgae by marine herbivores has been shown to increase with temperature and this increase in grazing can counter the positive effects of warming on plant growth (O’Connor 2009; Mrowicki and O’Connor 2015; Gutow et al. 2016). Marine herbivores have a strong impact on the abundance of primary producers globally, with the impacts of herbivores varying markedly among taxa of macroalgae and seagrasses (Poore et al. 2012). Feeding on macroalgae with low nutritional content, chemical defences, or both is known to profoundly affect herbivore fitness (Pennings and Carefoot 1995, Cruz-Rivera and Hay 2001).

Relatively a few studies have examined how variation among diets will affect marine herbivores in warming conditions (Table 2). Studies that have contrasted feeding rates or preferences among available algal resources have shown that feeding behaviour is dependent on temperature (e.g., feeding preferences of the amphipod Ampithoe longimana, Sotka and Giddens 2009; consumption rates of the urchin Lytechinus variegatus, Lemoine and Burkepile 2012). The few long-term studies that have simultaneously manipulated both diet and temperature during development have shown both independent and interactive responses to each factor (e.g., independent effects on copepod Temora longicornis, Boersma et al. 2016; interactive effects on copepod Acartia tonsa, Malzahn et al. 2016). Multi-generational studies with entire communities have demonstrated how changes to abundance and feeding due to climate stressors can alter trophic structure (e.g., Hale et al. 2011; Svensson et al. 2017).

In this study, we test how increased temperature and diets of varying quality for herbivore survival interact to determine the performance of the herbivorous marine amphipod, Sunamphitoe parmerong. We considered performance across multiple generations and response variables (short-term thermal tolerance, growth, feeding, survival, development rate, and fecundity). First, a thermal gradient was used to determine how short-term survival of S. parmerong varies with temperature. With short-term survival only reduced at extreme temperatures well beyond that currently experienced, we then raised multiple generations on different diets across a range of temperatures currently experienced annually and tolerated by amphipods in the short-term experiment. In the multi-generational experiment, we tested how growth, number of surviving offspring, and reproduction vary with increased temperature (ambient, + 2 and + 4 °C) and diet (three species of brown algae; Sargassum linearifolium, S. vestitum, and Colpomenia peregrina). The brown algal hosts for this herbivore vary strongly in nutritional quality, seasonal availability, and their suitability for herbivore survival (Poore and Steinberg 1999). We quantified per capita feeding rates on the same three diets under the same temperatures to address whether the observed patterns in survival were explained by differential feeding rates, and addressing the hypothesis that per capita consumption increases with warming (Fig. 1 details which possible temperature effects are tested across all experiments).

Materials and methods

Study organisms and collection

The amphipod Sunamphitoe parmerong (Poore and Lowry) is an abundant herbivore on subtidal rocky reefs in south-eastern Australia (recently transferred from the genus Peramphithoe by Peart and Ahyong 2016). This species feeds within nests made by rolling blades of its macroalgal hosts. In the Sydney region, S. parmerong occurs predominantly on the brown algae S. linearifolium (Turner) C. Agardh at mean densities of 0.4–2.2 individuals per gram of algae and Sargassum vestitum (R. Brown ex Turner) C. Agardh (0.3–0.8 per g), with lower numbers also occurring on C. peregrina (Sauvageau) Hamel (0–0.78 per g) and Padina crassa Yamada (0–1.2 per g) (minimum and maximum densities from bi-monthly samples in Poore and Steinberg 1999). All algae and amphipods used in experiments were collected from 1 to 4 m depth from two sites in Port Jackson (Sydney Harbour); Shark Bay (33°50′54.4″S, 151°16′6.08″E) and Chowder Bay (33°50′20.9″S, 151°15′16.8″E) and one site in coastal Sydney (Malabar, 33°57′54.6″S, 151°15′22.4″E). The sea surface temperatures (SST) in Sydney Harbour have an annual range of 15–25 °C as shown by logger data (HOBO TidbiT, Onset Comp. Corp., MA, USA) collected at 20 min intervals at ~ 3 m depth in the amphipod habitat at Chowder Bay (2013–2016) (Fig. S1). At the time of collection, the ambient temperature of the seawater at the collection sites was recorded.

For the short thermal tolerance study and feeding rate assay, S. vestitum and associated epifaunal communities were collected from Shark Bay, placed in resealable plastic bags, and promptly transferred to the laboratory in an insulated box where the S. parmerong were carefully removed by hand (considered as ‘field fresh’, using the terminology of Faulkner et al. 2014).

Tolerance of S. parmerong to short-term thermal stress

To determine the thermal tolerance limits of S. parmerong, field-fresh individuals were randomly allocated to a treatment across a gradient of 12 temperatures (20–34 °C) established using an aluminium temperature block. The thermal gradient across the block was established using hot- and cold-water inputs at either end (methods as per Hardy et al. 2014). Amphipods were placed in 30 ml glass vials of filtered seawater (1.0 µm, Millipore) at ambient temperature and then randomly placed in the wells of the temperature block. They were monitored until death/cessation of movement over 5 h. The experiment was repeated over 12 days (up to 92 animals collected per day) with a total of 201 S. parmerong assayed for thermal tolerance. The temperatures used included current thermal extremes in Sydney Harbour (Supplementary Fig. S1) and beyond near-future predictions of increasing sea surface temperatures (Hobday and Lough 2011; Doney et al. 2012). Pilot experiments had shown no mortality at temperatures below 20 °C.

The time to immobilization (Timm), when amphipod pleopods stopped beating, was recorded and the dead S. parmerong preserved in ethanol, sexed, and photographed. Total length was recorded as the curved line from where the antennae join to the head to the end of the telson from digital images using ImageJ (https://imagej.nih.gov/ij/). Kaplan–Meier survivorship curve analysis was used to estimate the proportional survival of animals over time, using the R package survival (Therneau 2015). A Cox Proportional Hazard model was used to test the effects of total length and sex of amphipods on survival.

Multi-generational effects of diet and temperature on S. parmerong survival and reproduction

To test how temperature affects the growth, survival, and fecundity of S. parmerong across multiple generations, and whether those effects interact with diet quality, we reared amphipods in a fully crossed combination of temperature (ambient = 17 °C, + 2 °C = 19 °C, + 4 °C = 21 °C) and algal diet (S. linearifolium, S. vestitum, C. peregrina) treatments. With short-term mortality only occurring at temperatures well above the current thermal extremes (see “Results”, Fig. 2), we used temperatures that reflected variation close to the current annual mean SST (20 °C, 2016) in Sydney Harbour (Fig. S1). These algal diets vary widely in quality for S. parmerong, with the previous research showing that survival on C. peregrina is approximately 50% of that on the species of Sargassum (Poore and Steinberg 1999).
Fig. 2

Survival of individual S. parmerong in the thermal stress experiment (scatter plot and fitted survival curve). The data points are the time to immobilization at static temperature, with the experiment ending after 300 min (n = 201). On the left, the grey bars indicate the number of days with a mean temperature above each of 20, 21, 22, 23, and 24 °C in 2015 (see Supplementary Fig. S1 for recent sea surface temperature data from Sydney Harbour)

Individual S. parmerong was collected from Shark Bay and placed in an outdoor aquaculture tank (500 L) with flowing ambient seawater at the Sydney Institute of Marine Sciences. Sixty brooding females were removed from this tank and isolated in individual 70 mL containers supplied with flowing seawater at ambient temperatures for a 48-h recovery period (97% survival) before being assigned to temperature treatments. They were randomly allocated to one of the nine combinations of temperature and diet treatments (n = 6 per treatment). The diet treatments consisted of algal pieces of approximately 2 cm2 in surface area of each of the three species.

Ambient and heated flowing seawater was pumped from automatic temperature-controlled header tanks (~ 60 L h−1) through a looped irrigation system that distributed water independently to individual containers. Containers were 70 ml plastic pots with a 2 cm2 square cut out from the wall with 280 µm mesh inserted. Drippers attached to the irrigation system distributed water 2 drops/second, approximately 360 mL h−1. For the + 2 °C and + 4 °C treatments, the temperatures were increased at a rate of 1 °C/12 h until treatment temperatures were reached.

The brooding females were monitored daily until moulting occurred, which forcibly ejects all hatched offspring from the maternal brood pouch. This was considered as day 0 for the F1 generation. Every 2 days, fresh algal pieces were added (food always in excess) and the containers cleaned of any faecal matter or detritus. With the food frequently replaced, this experimental design did not test for possible indirect effects of temperature on herbivores, mediated by changes to algal tissues grown under varying temperatures (Fig. 1). The females of the F0 generation were removed after 7 days, preserved in ethanol and their length measured. They were not removed immediately after moulting to avoid disturbing the newly hatched juveniles (which create their nests in close proximity to their mother, Poore and Steinberg 1999). The size of the females in the F0 generation was contrasted among treatments with analysis of variance, with temperature and diet as fixed, factorial factors.

The experiment ran until the F1 generation was 35 days old, by which time they were sexually mature. All individuals were removed from the containers and preserved in ethanol. We recorded the total number, size, and sex of surviving amphipods from the first generation (F1). The surviving females of the F1 generation included those that were brooding eggs, brooding hatched juveniles (that stay in the brood pouch for ~ 3–4 days), and those whose offspring had already left the brood pouch (the F2 generation). Consequently, we considered the sum of brooded eggs and newly hatched juveniles (in or out of the maternal brood pouch) as the potential F2 population size. The proportion of hatched juveniles in this F2 population (total brooded eggs and hatched juveniles) was calculated as a measure of development rate.

The number of individuals of the F1 generation and the potential F2 population size were each contrasted among treatments with a generalized linear model with temperature and diet as fixed, factorial factors and a Poisson error distribution. The size of F1 individuals and the number of eggs per F1 female (for those currently brooding eggs) were contrasted among treatments with a linear mixed model with temperature and diet as fixed, factorial factors, and individual containers as a random factor nested within each combination of treatments (in the R package lme4, Bates et al. 2015). The size of F0 females and proportion of F2 offspring that had hatched was contrasted among treatments and diets using factorial ANOVA. For significant effects, we tested for differences among levels of the categorical factors using Tukey’s post hoc tests in the R package multcomp (Hothorn et al. 2008). Statistical analyses were conducted in R (v. 3.3.3) and assumptions of all tests were checked by plots of the residuals versus fitted values.

Temperature and diet effects on feeding rate of S. parmerong

To test whether the population responses in the multi-generational experiment could be explained by temperature effects on feeding rates, we conducted a feeding rate experiment with the same temperature and diet combinations. Individual adult S. parmerong were collected from Shark Bay and randomly added to individual 70 ml plastic containers within each of the nine temperature and diet combinations (n = 6 per combination). The containers were filled with 50 ml of seawater and a pre-weighed piece of approximately 1 cm2 of either S. vestitum, S. linearifolium, or C. peregrina. Fifty-four containers without animals were used as autogenic controls for background loss in algal mass (n = 6 per treatment). The containers were moved to control temperature rooms and maintained at the treatment temperatures (17, 19, and 21 °C) for 48 h. Every 12 h, 25 ml of seawater was replaced along with the removal of detritus and faecal material. Light cycles were manipulated to reflect natural conditions. 95% of S. parmerong individuals survived the feeding assay.

At 48 h, remaining algal material was weighed and S. parmerong individuals preserved for sex determination and size measurements. To account for possible mass loss in the control treatments, consumption was estimated by the difference in mass loss in a grazed and a randomly paired control replicate of the same algal species and temperature. Consumption was contrasted among diets and temperature treatments with factorial ANOVA.

Tissue traits of algae in experimental treatments

While the replacement of food pieces, every 48 h in the multi-generational experiment was expected to prevent temperature effects on algal tissue qualities (and thus indirect temperature effects on herbivore performance), we checked this assumption by analyzing the C:N ratio, as a proxy for nutritional content, and the wet-to-dry mass ratio of algal pieces in experimental conditions. Algal pieces weighing approximately 2 g (wet weight) of each of the two Sargassum species were placed in treatment conditions for the same length of time that they were present in the multi-generational and consumption experiments. The wet mass of these tissues was recorded and then the dry mass after 48 h in a freeze dryer. The dried samples were then analyzed for carbon and nitrogen contents in a Flash EA Elemental Analyzer coupled to a Delta V plus isotope ratio mass spectrometer. C. peregrina was not used in these tissue analyses due to seasonal unavailability in the field at the time. The C:N and wet:dry mass ratios were contrasted between species and among temperatures with factorial ANOVA.

Results

Tolerance of S. parmerong to short-term thermal stress

The thermal tolerance of S. parmerong as indicated by time to death/immobility showed low or no mortality at temperatures between 20 and 26 °C after 300 min (Fig. 2). At temperatures higher than 27 °C, the time to immobilization (Timm) of S. parmerong decreased rapidly, with each additional degree of temperature decreasing the survival time by 16.7% (Fig. 2). Temperatures above 32 °C were lethal within minutes. The survival of S. parmerong did not vary significantly with their total length (X2 = 0.6, p = 0.74) or between males and females (X2 = 3.3, p = 0.19).

Multi-generational effects of diet and temperature on S. parmerong

At their first moult when releasing their brood of offspring, the females used to initiate the experiment (F0) were larger at higher temperatures (15% longer at + 4 °C than in ambient conditions (Fig. 3a, Table 1). These females were exposed to increased temperature for, on average, 16.7 ± 0.77 SE days before moulting. There were no effects of algal diet on size of F0 females, or interaction between diet and temperature (Table 1).
Fig. 3

a Total length of female S. parmerong after their first moult in each of the nine combinations of temperature (ambient, + 2 and + 4 °C) and diet (C. peregrina, S. linearifolium and S. vestitum). These were the females used to initiate the populations in each treatment (the F0 generation). b Size of the offspring of these females (the F1 generation). Data are mean ± SE (n = 2–5 per diet/temperature combination in a, n = 14–92 in b). Treatments that share a letter did not differ in Tukey’s post hoc tests

Table 1

Results from analyses of the temperature and diet treatments on the length, population size, development rate and brood size, and consumption over 48 h of S. parmerong in the experimental containers

Response variable

Factor

df

P

Length of F0 females

Temperature

2.23

0.02*

Diet

2.23

0.87

Temperature × diet

2.23

0.99

Number of F1 individuals

Temperature

2.42

0.16

Diet

2.40

< 0.001*

Temperature × diet

4.36

< 0.001*

Length of F1 individuals

Temperature

5.7

0.58

Diet

5.7

< 0.001*

Temperature × diet

7.11

0.75

Proportion of F2 juveniles hatched

Temperature

2.25

0.09

Diet

2.25

0.003*

Temperature × diet

4.25

0.52

Brood size of F1 females

Temperature

5.7

0.64

Diet

5.7

< 0.001*

Temperature × diet

7.11

0.99

Potential population size of F2 generation

Temperature

2.42

< 0.001*

Diet

2.40

< 0.001*

Temperature × diet

4.36

< 0.001*

Consumption of fresh algae

Temperature

2.41

0.01*

Diet

2.41

< 0.001*

Temperature × diet

4.41

0.53

The length of F0, proportion of F2 juveniles hatched and consumption were contrasted among treatments using analysis of variance with temperature and diet as fixed factorial factors. The number of individuals in the F1 generation and the potential population size of the F2 generation (sum of eggs, embryo, and newly hatched juveniles) were contrasted among treatments with generalized linear models with temperature and diet as fixed factorial factors and a Poisson error distribution. The length of all F1 individuals and the number of eggs per brooding female in the F1 generation were contrasted among treatments using linear mixed models with temperature and diet as fixed factorial factors, and individual container as a random factor nested within each combination of experimental treatments. Significant effects (P < 0.05) are marked with an asterisk

Thirty-five days after the females’ moult, the number of surviving amphipods in the F1 generation was affected by temperature only on certain diets (Fig. 4a, a significant temperature × diet interaction, Table 1). The number of individuals surviving on diets of C. peregrina was the lowest overall accounting for only 20% of the total surviving F1 offspring, with the highest number on the intermediate temperature (Fig. 4a). When consuming S. linearifolium, the number of surviving F1 offspring increased with increasing temperature, with the number in the + 4 °C treatment being, on average, 210% of the number in the ambient temperature. There were no effects of temperature on the number of surviving individuals on diets of S. vestitum (Fig. 4a). The size of the surviving F1 individuals varied among diets, but not with temperature, and there was no interaction between temperature and diet (Fig. 3b, Table 1). Amphipods reared on S. vestitum were of similar size to those reared on S. linearifolium and were 12% larger than those fed C. peregrina (Fig. 3b).
Fig. 4

a Number of S. parmerong offspring in the F1 generation and b the potential population size of the F2 generation in each of the nine combinations of temperature (ambient, + 2 and + 4 °C) and diet (C. peregrina, S. linearifolium, and S. vestitum). Data are mean ± SE (n = 5 per diet/temperature combination). Treatments that share a letter did not differ in Tukey’s post hoc tests

The potential population size of juveniles in the F2 generation (sum of brooded eggs, embryos, and newly hatched juveniles) varied among temperature treatments, with the effect differing strongly among diets (Fig. 4b, a significant temperature × diet interaction, Table 1). Amphipods reared on C. peregrina had the lowest F2 population size with 64% fewer eggs and juveniles than the other treatments and the highest numbers were in the intermediate temperature treatment (Fig. 4b). At 17 and 19 °C, the population size of the amphipod fed S. linearifolium did not differ from the best performing C. peregrina treatment, while at 21 °C, S. linearifolium supported an F2 population size 260% larger than lower temperatures (Fig. 4b). Amphipods reared on S. vestitum had twice the F2 population size in the ambient temperature treatment compared to other algal treatments (Fig. 4b).

There was no effect of temperature on the number of eggs per brooding female (Table 1), indicating that the temperature effects on the numbers of F1 and F2 amphipods (Fig. 4) were due to differences in survival rather than fecundity per capita. Fecundity, did, however, differ among diet treatments, with the females of the F1 generation reared on S. linearifolium and S. vestitum having larger brood sizes (22 and 44% larger on average, respectively), than those reared on the low-quality C. peregrina. Development rate was also altered by the effect of diet, with S. linearifolium and S. vestitum producing a proportion of hatched juveniles at 35 days across all temperature treatments that was 8.5 times greater than that for the reproductive females in the C. peregrina treatments that were mainly brooding eggs at the end of the experiment (Supplementary Fig. S2a).

The mean (± SE) water temperatures within the containers during the experiment were; ambient, 17.578 ± 0.149 °C; + 2 °C treatment, 19.072 + 0.348 °C; and + 4 °C treatment, 21.066 ± 0.362 °C (n = 111 measurements per treatment).

Temperature and diet effects on feeding rate of S. parmerong

Across all algal diets, temperature affected feeding rates, with mass loss due to consumption by S. parmerong highest at the intermediate temperature of 19 °C. At this temperature, mass loss was 35% higher, on average, than in the ambient 17 °C treatment and 60% higher than the 21 °C treatment (Fig. 5, Table 1). Amphipods consumed approximately five times more C. peregrina than the two species of Sargassum, that did not differ in consumption rates (Fig. 5). There was no interaction between algal diet and temperature (Table 1). The mean (± SE) water temperatures within the containers during the feeding assay were; ambient, 17.10 ± 0.02 °C; + 2 °C treatment, 19.49 + 0.02 °C; and + 4 °C treatment, 20.96 ± 0.06 °C (n = 4 measurements per container).
Fig. 5

Algal tissue consumed (mg fresh mass) in 48 h under each of the 9 combinations of temperature (ambient, + 2 and + 4 °C) and diet (C. peregrina, S. linearifolium, and S. vestitum). Data are mean ± SE (n = 4–6 per diet/temperature combination). Treatments that share a letter did not differ in Tukey’s post hoc tests

Tissue traits of algae in experimental treatments

There were no temperature effects on the C:N ratio of the algal material held in treatment conditions for the same time as those used to feed amphipods in the long-term growth experiment (F2,12 = 1.94, p = 0.29). The C:N ratio was significantly higher in S. vestitum than S. linearifolium (F1,12 = 87.96, p < 0.0001). The wet:dry ratio of algae tissues did not significantly differ between temperature treatments (F1, 72 = 0.002, p = 0.99).

Discussion

Experimental warming affected a marine plant–herbivore interaction by enhancing the survival of an herbivore consuming one of its major host plants. These effects, however, were not evident for this herbivore feeding on alternative diets, with temperature and diet strongly interacting to determine herbivore population size. Our results highlight the need to include variation in diet quality when predicting the impacts of climatic change, and that warming will potentially affect top–down control of plants by herbivores by changing their abundance in addition to any changes in the grazing rates of individuals.

Effects of increasing temperature on herbivore performance vary with diet

Both diet quality and temperature are expected to strongly affect the performance of herbivores (Manyak-Davis et al. 2013), but the degree to which these two factors may interact is poorly known. When temperatures were increased within the range that is experienced throughout the year by S. parmerong (17–21 °C), warming affected the number of surviving offspring of the marine amphipod S. parmerong across multiple generations, with the magnitude and direction of the effects highly dependent on diet.

The number of individuals in each generation was best explained by variation in survival on the different combinations of diet and temperature, rather than effects on individual size or fecundity. The size and brood size of their offspring (F1 generation) varied with diet rather than temperature and cannot explain the observed temperature effects on F1 and F2 population sizes. Other traits of S. parmerong were affected by temperature or diet independently. The rate of development was strongly affected by diet, but not temperature, with those females in the Sargassum treatments having a combination of brooded eggs and hatched juveniles at the end of the experiment, while very few of the eggs produced by females on C. peregrina diet had hatched. Patterns of survival were not simply explained by differences in per capita consumption rates at these temperatures. Feeding rates on the two species of Sargassum did not differ, and the highest consumption was observed when feeding on C. peregrina (consistent with the previous findings of compensatory feeding on this alga, Poore and Steinberg 1999).

Interactions between diet and temperature complicate predictions of how plant–herbivore interactions are likely to be altered in a changing climate. For example, fitness of the generalist beetle Popillia japonica is more strongly reduced by elevated temperatures when raised on low-quality plants compared to high-quality plants (Lemoine et al. 2013). The negative effects of food quality on fitness in herbivorous insects can be most pronounced at either high (e.g., Stamp and Bowers 1990) or low ambient temperatures (e.g., Stamp 1990; Diamond and Kingsolver 2010). The few previous experiments that have simultaneously manipulated both diet and temperature for marine herbivores have found that the effects of increasing temperature can vary in strength and/or direction across alternative diets (Table 2). The growth rates of planktonic copepods were more strongly affected by temperature when raised on low-quality food sources (Malzahn et al. 2016), while other experiments have found temperature and diet acting independently to affect herbivore fitness. For example, diet has a larger effect than temperature on the survival of the amphipod, Ampithoe longimana, with temperature affecting amphipod size (Sotka and Giddens 2009).
Table 2

Compilation of recent studies involving marine herbivores with experimental designs able to test for interactions between temperature and diet

Herbivore

Experimental treatments

Response variables

References

Consumption rate

Feeding preference

Growth

Survival

Fecundity

Multiple generations

Amphipod

Temperature, diet

T, D

 

T, D

T × D

D

T × D

Current study

Amphipod

Temperature, diet

T

T

    

Schram et al. (2015)

Copepod

Temperature, diet

  

T × D

   

Malzahn et al. (2016)

Copepod

Temperature, diet

 

T

    

Boersma et al. (2016)

Amphipod

Temperature, diet, area

T ×  D × area

Tns

T

D, area

Area

 

Sotka and Giddens (2009)

Amphipod

Temperature, pH

T × pH

 

T

T, pH

  

Schram et al. (2016)

Gastropod

Temperature, pH

T

  

T

  

Cardoso et al. (2017)

Amphipod

Temperature, diet, pH

T × pH

 

T, pH

T, pH

  

Poore et al. (2013)

Urchin

Temperature, diet, pH

T, D, pH

     

Burnell et al. (2013)

Isopod

Temperature

T

     

Gutow et al. (2016)

Urchin

Temperature

T

 

T

   

Watts et al. (2011)

Urchin

Temperature

T

     

Lemoine and Burkepile (2012)

Studies are those that have (a) manipulated both temperature and diet simultaneously, or (b) manipulated temperature and then measured the responses of herbivores to diet treatments. For each main category of response variables, we indicate whether the individual treatment affected the response (T, temperature; D, diet; T × D, a temperature × diet interaction) or had no significant effect (e.g., Tns). Empty cells indicate that the response variable was not measured in that study

Patterns in herbivore or plant traits that might explain these disparate results are elusive, suggesting that it remains difficult to predict when and how temperature and food quality will interact generally among ectothermic herbivores. Theory predicts a wide variety of possible interactions depending on whether consumers are energy or nutrient limited, and whether the quality of resources is also affected by temperature (Cross et al. 2015). Temperature effects on nitrogen metabolism (e.g., Lemoine and Shantz 2016) or the ability to detoxify secondary metabolites (Sotka and Giddens 2009) could all give rise to diet by temperature interactions. In this study, the three diets differ in their tissue qualities with C. peregrina having a high water content and low nitrogen content relative to the two species of Sargassum (Poore and Steinberg 1999), and the Sargassum species differing in C:N ratio (higher in S. vestitum) and levels of potentially deterrent secondary metabolites (phlorotannin content higher in S. vestitum, Steinberg and van Altena 1992). With algal pieces being consumed or replaced within 2 days, our experiment was not designed to detect indirect effects on herbivores due to altered tissue qualities. Increased temperature can alter the nutritional value and concentration of secondary metabolites in brown algal tissues (e.g., C:N ratio, Staehr and Wernberg 2009), but we found no temperature effects on water content and C:N ratio of the Sargassum spp. pieces subject to the same temperature treatments. These results are consistent with the previous studies, showing that warming by 4 °C did not alter the palatability of S. vestitum to an herbivorous gastropod (Poore et al. 2016) and that warming by 5 °C did not alter nitrogen and phlorotannin concentration of S. linearifolium (Phelps et al. 2017).

Integrating results across studies is also complicated by the variation in ambient and elevated temperatures used among experiments. For S. parmerong, temperatures above 27 °C rapidly lead to mortality (this study, and in the previous experiments with this species, Poore et al. 2013). While the frequency of thermal extremes in south-eastern Australia is predicted to increase in future years (King et al. 2017) and heat waves have striking effects on temperate marine communities (Wernberg et al. 2013), there is also a need to understand how changes to mean temperatures are likely to affect herbivore populations. The temperatures used in this long-term experiment are those well within the annual range of temperatures in Sydney Harbour and experienced by S. parmerong for long periods within the year. Increased mean temperatures may thus benefit this herbivore by increasing the number of S. parmerong on one of its two main algal hosts. Warming can clearly act as either a stress or a benefit to marine organisms depending on the context (Goldenberg et al. 2017).

Temperature effects on likely top–down control of macroalgae

Metabolic theory predicts that grazing rates will increase under warmer conditions and strengthen plant–herbivore interactions due to a mismatch between the rates in which temperature affects consumers and primary production (O’Connor 2009). In marine herbivores, this prediction is supported by experiments with single diets (e.g., O’Connor 2009; Gutow et al. 2016; Cardoso et al. 2017). Increased temperature, however, can also shift herbivore preferences among alternative diets (Schram et al. 2015; Boersma et al. 2016), and may interact with diet quality to affect per capita consumption rates. The results of our feeding assay showed that increasing temperature from 17 to 19 °C increased per capita feeding rates, but these then declined at 21 °C and we found no interaction with diet. The much larger temperature effects on population size, however, suggest that grazer impacts on macroalgae in this system would increase in warmed conditions—expected to increase linearly with consumer biomass in the absence of any density-dependent effects on individual behaviour (Atkins et al. 2015). In a similar study system of amphipods grazing on macroalgae, Heldt et al. (2016) demonstrated that future conditions of temperature and pH resulted in large increases in secondary productivity, due to relaxed constraints on amphipod fecundity. While multiple diets were not considered in their design, the potential for increased population sizes in a changing ocean shows the importance of measuring fecundity and survival in addition to short-term measures of grazing rates. Predicting the future levels of top–down control of algae by herbivores in a given environment, however, also requires an understanding of variation among local herbivore species (Table 2), how temperature can affect the predator control of herbivore populations, and how temperature affects the abundance and quality of primary producers (Fig. 1; Lemoine et al. 2013; Poore et al. 2013; Cross et al. 2015).

Experiments that only measure short-term responses to thermal extremes are useful for predicting the impacts of marine heat waves, but cannot capture the longer term effects of temperature variation on growth, survival, and fecundity. The methods used to establish thermal maxima have been inconsistent, ranging from dynamic rates of warming to static temperature tests (as found in our experiment), and acclimation can result in overestimating mismatches in measured processes (Faulkner et al. 2014; Lemoine and Burkepile 2012). Long-term experiments with herbivores on natural diets integrate multiple processes to better predict the impacts of climate change, given that diet can modify temperature effects (this study, Malzahn et al. 2016), and that grazers can mediate the direct and indirect responses of climate stressors on primary production (Alsterberg et al. 2013). In this study system, S. parmerong reproduce continually, within population sizes on available hosts varying across the year due to spatial and temporal variation in algal availability (Poore and Steinberg 1999). In common with other generalist herbivores, individuals may be constrained to a single diet due to the patchiness of available plants in space and their availability in time (Fox and Morrow 1981). The two species of Sargassum vary widely in biomass across the year, and alternative hosts (including C. peregrina and Padina crassa) are only abundant in some months (Poore and Steinberg 1999). We ran our long-term experiment in the cooler months, and further experiments are needed to predict how diet quality may interact with temperatures closer to the thermal maximum for this species. With warming predicted to negatively affect large brown algae, but benefit turfing algae (Connell and Russell 2010), climate change is likely to affect the temporal availability of algae, and thus, the time spent on alternative hosts.

With altered interactions among species likely to be one of the most important outcomes of climatic change in the ocean (Kordas et al. 2011; Vergés et al. 2014; Gaylord et al. 2015), studies are needed that consider multiple trophic levels on time scales able to detect both individual and population level changes, and changes to trophic structure (e.g., Svensson et al. 2017). Given the very strong top–down control of primary producers by marine herbivores (Poore et al. 2012), any changes to the abundance of herbivores and/or their feeding behaviour can strongly reshape community structure. The results from this study show that the effects of temperature on multiple generations of a marine herbivore are strongly dependent on resource availability (algal diet). Furthermore, the effects of temperature were only evident with some measures of herbivore performance, emphasizing the need to combine both short- and long-term experiments on communities in changing environmental conditions.

Notes

Acknowledgements

This research was supported by a Grant from the Australian Research Council (DP150102771). We thank S. Dworjanyn (Southern Cross University) for the assistance with carbon and nitrogen measurements, E. Sotka (College of Charleston) for comments that improved this manuscript, N. Coombes and A. Niccum (Sydney Institute of Marine Science) for the help with aquarium facilities, T. Stelling-Wood, B. Lanham, and L. Martin (University of New South Wales) for the experiment and field support, and J. Harianto (University of Sydney) for harbour temperature data. We thank C. Müller and three anonymous reviewers for comments that improved this manuscript.

Author contribution statement

JL, MB, and AGBP conceived and designed the experiments. JL performed the experiments and analyzed the data. JL and AGBP wrote the manuscript and MB provided editorial contributions.

Supplementary material

442_2018_4084_MOESM1_ESM.docx (205 kb)
Supplementary material 1 (DOCX 205 kb)

References

  1. Alsterberg C, Eklöf JS, Gamfeldt L, Havenhand JN, Sundbäck K (2013) Consumers mediate the effects of experimental ocean acidification and warming on primary producers. Proc Natl Acad Sci USA 110(21):8603–8608.  https://doi.org/10.1073/pnas.1303797110 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Atkins RL, Griffin JN, Angelini C, O’Connor MI, Silliman BR (2015) Consumer-plant interaction strength: importance of body size, density and metabolic biomass. Oikos 124:1274–1281.  https://doi.org/10.1111/oik.01966 CrossRefGoogle Scholar
  3. Bates D, Mächler M, Bolker BM, Walker SC (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  4. Boersma M, Mathew KA, Niehoff B, Schoo KL, Franco-Santos RM, Meunier CL (2016) Temperature driven changes in the diet preference of omnivorous copepods: no more meat when it’s hot? Ecol Lett 19:45–53.  https://doi.org/10.1111/ele.12541 CrossRefPubMedGoogle Scholar
  5. Burnaford JL (2004) habitat modification and refuge from sublethal stress drive a marine plant–herbivore association. Ecology 85:2837–2849CrossRefGoogle Scholar
  6. Burnell OW, Russell BD, Irving AD, Connell SD (2013) Eutrophication offsets increased sea urchin grazing on seagrass caused by ocean warming and acidification. Mar Ecol Prog Ser 485:37–46.  https://doi.org/10.3354/meps10323 CrossRefGoogle Scholar
  7. Burrows MT, Schoeman DS, Buckley LB, Moore P, Poloczanska ES, Brander KM, Brown C, Bruno JF, Duarte CM, Halpern BS, Holding J, Kappel CV, Kiessling W, O’Connor MI, Pandolfi JM, Parmesan C, Schwing FB, Sydeman WJ, Richardson AJ (2011) The pace of shifting climate in marine and terrestrial ecosystems. Science 334:652–655.  https://doi.org/10.1126/science.1210288 CrossRefPubMedGoogle Scholar
  8. Cardoso PG, Grilo TF, Dionísio G, Aurélio M, Lopes AR, Pereira R, Pacheco M, Rosa R (2017) Short-term effects of increased temperature and lowered pH on a temperate grazer-seaweed interaction. Estuar Coast Shelf Sci 197:35–44.  https://doi.org/10.1016/j.ecss.2017.08.007 CrossRefGoogle Scholar
  9. Cleland EE, Chuine I, Menzel A, Mooney HA, Schwartz MD (2007) Shifting plant phenology in response to global change. Trends Ecol Evol 22:357–365.  https://doi.org/10.1016/j.tree.2007.04.003 CrossRefPubMedGoogle Scholar
  10. Connell SD, Russell BD (2010) The direct effects of increasing CO2 and temperature on non-calcifying organisms: increasing the potential for phase shifts in kelp forests. Proc R Soc B Biol Sci.  https://doi.org/10.1098/rspb.2009.2069 CrossRefGoogle Scholar
  11. Cross WF, Hood JM, Benstead JP, Huryn AD, Nelson D (2015) Interactions between temperature and nutrients across levels of ecological organization. Glob Change Biol 21:1025–1040.  https://doi.org/10.1111/gcb.12809 CrossRefGoogle Scholar
  12. Cruz-Rivera E, Hay ME (2001) Macroalgal traits and the feeding and fitness of an herbivorous amphipod: the roles of selectivity, mixing, and compensation. Mar Ecol Prog Ser 218:249–266CrossRefGoogle Scholar
  13. Davis AJ, Lawton JH, Shorrocks B, Jenkinson LS (1998) Individualistic species responses invalidate simple physiological models of community dynamics under global environmental change. J Anim Ecol 67:600–612CrossRefGoogle Scholar
  14. Diamond SE, Kingsolver JG (2010) Fitness consequences of host plant choice: a field experiment. Oikos 119:542–550.  https://doi.org/10.1111/j.1600-0706.2009.17242.x CrossRefGoogle Scholar
  15. Doney SC, Ruckelshaus M, Duffy JE, Barry JP, Chan F, English CA, Galindo HM, Grebmeier JM, Hollowed AB, Knowlton N, Polovina J, Rabalais NN, Sydeman WJ, Talley LD (2012) Climate change impacts on marine ecosystems. Ann Rev Mar Sci 4:11–37.  https://doi.org/10.1146/annurev-marine-041911-111611 CrossRefPubMedGoogle Scholar
  16. Eisenlord ME, Groner ML, Yoshioka RM, Elliott J, Maynard J, Fradkin S, Turner M, Pyne K, Rivlin N, Van Hooidonk R, Harvell CD (2016) Ochre star mortality during the 2014 wasting disease epizootic: role of population size structure and temperature. Phil Trans R Soc B 371:20150212.  https://doi.org/10.1098/rstb.2015.0212 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Faulkner KT, Clusella-Trullas S, Peck LS, Chown SL (2014) Lack of coherence in the warming responses of marine crustaceans. Funct Ecol 28:895–903.  https://doi.org/10.1111/1365-2435.12219 CrossRefGoogle Scholar
  18. Fox LA, Morrow PA (1981) Specialization: species property or local phenomenon. Science 211:887–893CrossRefPubMedGoogle Scholar
  19. Gaylord B, Kroeker KJ, Sunday JM, Anderson KM, Barry JP, Brown NE, Connell SD, Fabricius KE, Hall-Spencer JM, Klinger T, Milazzo M, Munday PL, Russell BD, Sanford E, Scheriber SJ, Thiyagarajan V, Vaughan MLH, Widdicombe S, Harley CDG (2015) Ocean acidification through the lens of ecological theory. Ecology 96:3–15.  https://doi.org/10.1890/14-0802.1v CrossRefPubMedGoogle Scholar
  20. Goldenberg SU, Nagelkerken I, Ferreira CM, Ullah H, Connell SD (2017) Boosted food web productivity through ocean acidification collapses under warming. Glob Change Biol 23:4177–4184.  https://doi.org/10.1890/14-0802.1 CrossRefGoogle Scholar
  21. Gutow L, Petersen I, Bartl K, Huenerlage K (2016) Marine meso-herbivore consumption scales faster with temperature than seaweed primary production. J Exp Mar Biol Ecol 477:80–85.  https://doi.org/10.1016/j.jembe.2016.01.009 CrossRefGoogle Scholar
  22. Hale R, Calosi P, McNeill L, Mieszkowska N, Widdicombe S (2011) Predicted levels of future ocean acidification and temperature rise could alter community structure and biodiversity in marine benthic communities. Oikos 120:661–674.  https://doi.org/10.1111/j.1600-0706.2010.19469.x CrossRefGoogle Scholar
  23. Hardy NA, Lamare M, Uthicke S, Wolfe K, Doo S, Dworjanyn S, Byrne M (2014) Thermal tolerance of early development in tropical and temperate sea urchins: inferences for the tropicalization of eastern Australia. Mar Biol 161:395–409.  https://doi.org/10.1007/s00227-013-2344-z CrossRefGoogle Scholar
  24. Heldt KA, Connell SD, Anderson K, Russell BD, Munguia P (2016) Future climate stimulates population out-breaks by relaxing constraints on reproduction. Sci Rep 6:33383.  https://doi.org/10.1038/srep33383 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Helmuth B, Kingsolver JG, Carrington E (2005) Biophysics, physiological ecology, and climate change: does mechanism matter? Annu Rev Physiol 67:177–201.  https://doi.org/10.1146/annurev.physiol.67.040403.105027 CrossRefPubMedGoogle Scholar
  26. Hobday AJ, Lough JM (2011) Projected climate change in Australian marine and freshwater environments. Mar Freshw Res 62:1000–1014.  https://doi.org/10.1071/MF10302 CrossRefGoogle Scholar
  27. Hothorn T, Bretz F, Westfall P (2008) Simultaneous inference in general parametric models. Biom J 50:346–363.  https://doi.org/10.1002/bimj.200810425 CrossRefPubMedGoogle Scholar
  28. King AD, Karoly DJ, Henley BJ (2017) Australian climate extremes at 1.5 °C and 2 °C of global warming. Nat Clim Change 7:412–416.  https://doi.org/10.1038/nclimate3296 CrossRefGoogle Scholar
  29. Kingsolver JG, Huey RB (2008) Size, temperature, and fitness: three rules. Evol Ecol Res 10:251–268Google Scholar
  30. Kordas RL, Harley CDG, Connor MIO (2011) Community ecology in a warming world: the influence of temperature on interspecific interactions in marine systems. J Exp Mar Bio Ecol 400:218–226.  https://doi.org/10.1016/j.jembe.2011.02.029 CrossRefGoogle Scholar
  31. Lee KP, Roh C (2010) Temperature-by-nutrient interactions affecting growth rate in an insect ectotherm. Entomol Exp Appl 136:151–163.  https://doi.org/10.1111/j.1570-7458.2010.01018.x CrossRefGoogle Scholar
  32. Lemoine NP, Burkepile DE (2012) Temperature-induced mismatches between consumption and metabolism reduce consumer fitness. Ecology 93:2483–2489.  https://doi.org/10.1890/12-0375.1 CrossRefPubMedGoogle Scholar
  33. Lemoine NP, Shantz AA (2016) Increased temperature causes protein limitation by reducing the efficiency of nitrogen digestion in the ectothermic herbivore Spodoptera exigua. Physiol Entomol 41:143–151.  https://doi.org/10.1111/phen.12138 CrossRefGoogle Scholar
  34. Lemoine NP, Drews WA, Burkepile DE, Parker JD (2013) Increased temperature alters feeding behavior of a generalist herbivore. Oikos 122:1669–1678.  https://doi.org/10.1111/j.1600-0706.2013.00457.x CrossRefGoogle Scholar
  35. Malzahn AM, Doerfler D, Boersma M (2016) Junk food gets healthier when it’s warm. Limnol Oceanogr 61:1677–1685.  https://doi.org/10.1002/lno.10330 CrossRefGoogle Scholar
  36. Manyak-Davis A, Bell TM, Sotka EE (2013) The relative importance of predation risk and water temperature in maintaining Bergmann’s rule in a marine ectotherm. Am Nat 182:347–358.  https://doi.org/10.1086/671170 CrossRefPubMedGoogle Scholar
  37. Mrowicki R, O’Connor N (2015) Wave action modifies the effects of consumer diversity and warming on algal assemblages. Ecology 96:1020–1029.  https://doi.org/10.1890/14-0577.1 CrossRefPubMedGoogle Scholar
  38. O’Connor MI (2009) Warming strengthens an herbivore–plant interaction. Ecology 90:388–398CrossRefPubMedGoogle Scholar
  39. Ockendon N, Baker DJ, Carr JA, White EC, Almond REA, Amano T, Bertram E, Bradbury RB, Bradley C, Butchart SHM, Doswald N, Foden W, Gill DJC, Green RE, Sutherland WJ, Tanner EVJ, Pearce-Higgins JW (2014) Mechanisms underpinning climatic impacts on natural populations: altered species interactions are more important than direct effects. Glob Change Biol 20:2221–2229.  https://doi.org/10.1111/gcb.12559 CrossRefGoogle Scholar
  40. Peart RA, Ahyong ST (2016) Phylogenetic analysis of the family Ampithoidae Stebbing, 1899 (Crustacea: Amphipoda), with a synopsis of the genera. J Crust Biol 36:456–474.  https://doi.org/10.1163/1937240X-00002449 CrossRefGoogle Scholar
  41. Pecl GT, Araújo MB, Bell JD, Blanchard J, Bonebrake TC, Chen I-C, Clark TD, Colwell RK, Danielsen F, Evengård B, Falconi L, Ferrier S, Frusher S, Garcia RA, Griffis RB, Hobday AJ, Janion-Scheepers C, Jarzyna MA, Jennings S, Lenoir J, Linnetved HI, Martin VY, McCormack PC, McDonald J, Mitchell NJ, Mustonen T, Pandolfi JM, Pettorelli N, Popova E, Robinson SA, Scheffers BR, Shaw JD, Sorte CJB, Strugnell JM, Sunday JM, Tuanmu M-N, Vergés A, Villanueva C, Wernberg T, Wapstra E, Williams SE (2017) Biodiversity redistribution under climate change: Impacts on ecosystems and human well-being. Science 355:eaai9214.  https://doi.org/10.1126/science.aai9214 CrossRefPubMedGoogle Scholar
  42. Pennings SC, Carefoot TH (1995) Post-ingestive consequences of consuming secondary metabolites in sea hares (Gastropoda: Opisthobranchia). Comp Biochem Physiol Part C Comp 111:249–256CrossRefGoogle Scholar
  43. Phelps CM, Boyce MC, Huggett MJ (2017) Future climate change scenarios differentially affect three abundant algal species in southwestern Australia. Mar Environ Res 126:69–80.  https://doi.org/10.1016/j.marenvres.2017.02.008 CrossRefPubMedGoogle Scholar
  44. Poore AGB, Steinberg PD (1999) Preference-performance relationships and effects of host plant choice in an herbivorous marine amphipod. Ecol Monogr 69:443–464Google Scholar
  45. Poore AGB, Campbell AH, Coleman RA, Edgar GJ, Jormalainen V, Reynolds PL, Sotka EE, Stachowicz JJ, Taylor RB, Vanderklift MA, Emmett Duffy J (2012) Global patterns in the impact of marine herbivores on benthic primary producers. Ecol Lett 15:912–922.  https://doi.org/10.1111/j.1461-0248.2012.01804.x CrossRefPubMedGoogle Scholar
  46. Poore AGB, Graba-Landry A, Favret M, Sheppard Brennand H, Byrne M, Dworjanyn SA (2013) Direct and indirect effects of ocean acidification and warming on a marine plant-herbivore interaction. Oecologia 173:1113–1124.  https://doi.org/10.1007/s00442-013-2683-y CrossRefPubMedGoogle Scholar
  47. Poore AGB, Graham SE, Byrne M, Dworjanyn SA (2016) Effects of ocean warming and lowered pH on algal growth and palatability to a grazing gastropod. Mar Biol 163:99.  https://doi.org/10.1007/s00227-016-2878-y CrossRefGoogle Scholar
  48. Schram JB, McClintock JB, Amsler CD, Baker BJ (2015) Impacts of acute elevated seawater temperature on the feeding preferences of an Antarctic amphipod toward chemically deterrent macroalgae. Mar Biol 162:425–433.  https://doi.org/10.1007/s00227-014-2590-8 CrossRefGoogle Scholar
  49. Schram JB, Schoenrock KM, McClintock JB, Amsler CD, Angus RA (2016) Seawater acidification more than warming presents a challenge for two Antarctic macroalgal-associated amphipods. Mar Ecol Prog Ser 554:81–97.  https://doi.org/10.3354/meps11814 CrossRefGoogle Scholar
  50. Sotka EE, Giddens H (2009) Seawater temperature alters feeding discrimination by cold-temperate but not subtropical individuals of an ectothermic herbivore. Biol Bull 216:75–84.  https://doi.org/10.2307/25470725 CrossRefPubMedGoogle Scholar
  51. Sotka EE, Reynolds PL (2011) Rapid experimental shift in host use traits of a polyphagous marine herbivore reveals fitness costs on alternative hosts. Evol Ecol 25:1335–1355.  https://doi.org/10.1007/s10682-011-9473-y CrossRefGoogle Scholar
  52. Staehr PA, Wernberg T (2009) Physiological responses of Ecklonia radiata (Laminariales) to a latitudinal gradient in ocean temperature. J Phycol 45:91–99.  https://doi.org/10.1111/j.1529-8817.2008.00635.x CrossRefPubMedGoogle Scholar
  53. Stamp NE (1990) Growth versus molting time of caterpillars as a function of temperature, nutrient concentration and the phenolic rutin. Oecologia 82:107–113CrossRefPubMedGoogle Scholar
  54. Stamp N, Bowers MD (1990) Variation in food quality and temperature constrain foraging of gregarious caterpillars. Ecology 71:1031–1039CrossRefGoogle Scholar
  55. Stamp NE, Yang Y (1996) Response of insect herbivores to multiple allelochemicals under different thermal regimes. Ecology 77:1088–1102CrossRefGoogle Scholar
  56. Steinberg PD, van Altena I (1992) Tolerance of marine invertebrate herbivores to brown algal phlorotannins in temperate Australasia. Ecol Monogr 62:189–222CrossRefGoogle Scholar
  57. Svensson F, Karlsson E, Gårdmark A, Olsson J, Adill A, Zie J, Snoeijs P, Eklöf JS, Svensson F (2017) In situ warming strengthens trophic cascades in a coastal food web. Oikos.  https://doi.org/10.1111/oik.03773 CrossRefGoogle Scholar
  58. Therneau T (2015) A package for survival analysis in S. version 2.38, https://CRAN.R-project.org/package=survival
  59. Tylianakis JM, Didham RK, Bascompte J, Wardle DA (2008) Global change and species interactions in terrestrial ecosystems. Ecol Lett 11:1351–1363.  https://doi.org/10.1111/j.1461-0248.2008.01250.x CrossRefPubMedGoogle Scholar
  60. Vergés A, Steinberg PD, Hay ME, Poore AGB, Campbell AH, Ballesteros E, Heck KL Jr, Langlois T, Marzinelli EM, Mizerek T, Mumby PJ, Nakamura Y, Roughan M, Van Sebille E, Sen Gupta A, Smale DA, Tomas F, Wernberg T, Wilson SK (2014) The tropicalization of temperate marine ecosystems: climate-mediated changes in herbivory and community phase shifts. Proc R Soc B 281:20140846.  https://doi.org/10.1098/rspb.2014.0846 CrossRefPubMedPubMedCentralGoogle Scholar
  61. Watts SA, Hofer SC, Desmond RA, Lawrence AL, Lawrence JM (2011) The effect of temperature on feeding and growth characteristics of the sea urchin Lytechinus variegatus fed a formulated feed. J Exp Mar Biol Ecol 397:188–195.  https://doi.org/10.1016/j.jembe.2010.10.007 CrossRefGoogle Scholar
  62. Wernberg T, Smale DA, Tuya F, Thomsen MS, Langlois TJ, De Bettignies T, Bennett S, Rousseaux CS (2013) An extreme climatic event alters marine ecosystem structure in a global biodiversity hotspot. Nat Clim Change 3:78.  https://doi.org/10.1038/nclimate1627 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Evolution and Ecology Research Centre, School of Biological, Earth and Environmental SciencesUniversity of New South WalesSydneyAustralia
  2. 2.School of Medical Sciences and School of Life and School of Environmental SciencesUniversity of SydneySydneyAustralia

Personalised recommendations